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Article DOI: http://dx.doi.org/10.3201/eid2104.141415
Global Avian Influenza Surveillance in Wild
Birds: A Strategy to Capture Viral Diversity
Technical Appendix
Global Avian Influenza Surveillance in Wild Birds
Methods
We analyzed data from 1) a survey of the Organisation for Animal Health (OIE) member
countries conducted by OIE, 2) official OIE animal health reports from member countries by
using the World Animal Health Information Database (WAHID) interface (http://oie.int/wahid)
and the WAHID-Wild interface (http://oie.int/wahidwild); 3) reports of avian influenza wild bird
surveillance results published in the peer-reviewed literature by using the Web of Knowledge;
and 4) the Influenza Research Database (http://www.fludb.org).
OIE Member Survey
Influenza caused by H7N5 subtype virus that is affecting humans in China is not causing
clinical disease in birds. Thus, more proactive approaches to surveillance in birds are necessary
to detect viral infection. To determine the scope of current surveillance activities in wild birds, in
April 2013, the OIE asked all 178 member countries to provide information on surveillance
activities for avian influenza (caused by low pathogenic and highly pathogenic influenza viruses)
during the previous 12 months. Results received from 46 of 178 member countries were
reviewed.
OIE WAHID Interface Data
We also reviewed avian influenza reporting from the disease timeline database on the
WAHID interface (www.oie.int/wahid) during 2008–2012 by using data provided by OIE
member countries (data for 2013 were was not available at the time of analysis). Reporting of
Page 2 of 13
avian influenza virus subtypes H5, H7, and highly pathogenic avian influenza virus identified in
wild birds to OIE is mandated, and reporting of other subtypes of low pathogenic avian influenza
virus is voluntary as part of the OIE Worldwide Monitoring System for Wild Animals. For the
purposes of identifying countries reporting surveillance activities for this analysis, we included
countries reporting any of the following occurrence categories: confirmed infection but not
clinical disease, suspected, confirmed clinical disease, infection/infestation in ≥1 zones, or
clinical disease limited to ≥1 zones, disease suspected but not confirmed limited to ≥1 zones, or
absent.
Influenza Research Database
To determine other sources of information on avian influenza surveillance in wild birds
from outside sources (or potentially in conjunction with) reporting to OIE, we collected wild
avian surveillance data from the Influenza Research Database (http://www.fludb.org/) by using a
2-step approach. First, we conducted a search on November 26, 2013, on the Avian Surveillance
Summary Search (an option under Search Data→Animal Surveillance) refined for the host type
parameter Wild. The search excluded avian surveillance records categorized as captive wild or
domestic host type. Total wild bird counts per country were summed. Entries for countries with n
= 0 wild bird counts were excluded. By our definition (n>0 wild bird counts per country), reports
of avian influenza viruses originating from 40 countries were found. Second, by using the
Animal Surveillance Search page, we set display type to customizable summary table. Country
was selected as the primary y-axis attribute, and collection year was selected as the primary x-
axis attribute. The remaining default search settings were used. The resulting table displayed
years with sampling data for each country. For the 40 countries from which there were reports of
n>0 wild bird counts, data records were reviewed to determine if wild birds were sampled during
January 2008–June 2013 (collection date). Individual collection records were reviewed to ensure
that the records reflected n>0 wild birds as opposed to captive wild or domestic birds (noted as
behavior classification in the collection record) during the time frame. Most of total effort
(sample collection) for countries was reported during 2008–2013.
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Web of Knowledge
To explore the extent of reporting on avian influenza surveillance in wild birds in the
scientific literature, we searched the Thompson Reuters Web of Knowledge system (www.
webofknowledge.com) version 5.12 (all databases) on November 27, 2013, topic search term
[Avian Influenza] with publication date parameters for 2008–2013. The search yielded 20,757
results. The search was refined for search term wild bird and yielded 1,220 results. The search
was further refined for surveillance, which yielded 431 results. We limited inclusion of reports to
those conducting surveillance during 2008–2013. Abstracts were reviewed for surveillance time
frames and to confirm n>0 wild bird sampling in the country(s). When results were not clear, full
texts were reviewed. Papers needing more review without full-text online versions were searched
by using Google Scholar (www.scholar.google.com); if not available on either system, they were
not included. Publications focused on surveillance of domestic animals involving experimental
infection or investigating surveillance or testing method validation were excluded. In general,
information was not included from review papers, except where it was explicit that wild birds
had been sampled in a given country within the specified time frame. The list of countries from
which reports of conducting wild bird surveillance during January 2008–January 2013 by an
article available on Web of Knowledge was compiled (online Appendix Table). Information
matching the headings of the OIE survey was also extracted for a subset of 26 countries not
responding to the OIE survey but still reporting in the literature available on Web of Knowledge
to gain a sense of their sampling, testing, and reporting approaches.
Table. Current and recent surveillance for avian influenza virus in wild birds, by country and income level, reported surveillance by
country*
Income level, country
OIE survey
Reporting to OIE
Web of Knowledge
Influenza Research
Database
High
Australia
X
NR
X (1,2)
X
Austria
NR
X
X (3)
NR
Bahrain
NR
X
NR
NR
Belgium
X
X
NR
NR
Canada
X
X
X (4,5)
X
Chile
NR
X
NR
NR
Taiwan
X
X
NR
X
Croatia
NR
X
NR
NR
Czech Republic
X
X
X (6)
NR
Denmark
X
X
X (7)
NR
Equatorial Guinea
NR
X
NR
NR
Estonia
NR
X
NR
NR
Finland
X
X
NR
NR
France
NR
X
X (8)
NR
Germany
NR
X
X (3,9)
NR
Guadeloupe
NR
NR
X (10)
NR
Page 4 of 13
Income level, country
OIE survey
Reporting to OIE
Web of Knowledge
Influenza Research
Database
Hong Kong
NR
NR
X (11,12)
NR
Ireland
NR
X
NR
NR
Israel
NR
X
NR
NR
Italy
X
X
X (13,14)
NR
Japan
X
X
X (15–21)
X
South Korea
X
X
X (22–28)
NR
Kuwait
NR
X
NR
NR
Latvia
NR
NR
NR
X
Lithuania
NR
NR
X (29)
X
the Netherlands
NR
X
X (30)
X
New Caledonia
NR
X
NR
NR
New Zealand
X
X
NR
NR
Norway
X
X
X (31)
NR
Oman
NR
NR
NR
X
Poland
X
X
X (32,33)
NR
Portugal
X
X
X (34,35)
NR
Russia
NR
NR
X (36–38)
X
San Marino
NR
X
NR
NR
Saudi Arabia
NR
X
NR
NR
Singapore
X
X
NR
NR
Slovakia
NR
X
X (39)
NR
Slovenia
X
X
X (40)
NR
Spain
X
X
X (41)
NR
Sweden
NR
X
NR
NR
Switzerland
NR
NR
X (3,42)
NR
United Kingdom
X
X
X (43,44)
NR
United States
X
X
X (5,44–51)
X
Uruguay
NR
X
NR
NR
Upper middle
Algeria
NR
X
NR
NR
Argentina
X
X
X (52)
NR
Azerbaijan
NR
X
NR
NR
Bosnia and Herzegovina
X
X
NR
NR
Botswana
NR
X
X (53,54)
NR
Brazil
NR
X
NR
NR
Bulgaria
NR
X
X (55)
X
China
NR
X
X (56,57)
X
Colombia
X
NR
NR
X
Greece
X
NR
NR
X
Greenland
NR
NR
X (7)
X
Hungary
X
X
NR
X
Iceland
NR
X
NR
X
Iraq
X
NR
NR
NR
Kazakhstan
X
NR
X (38)
NR
Lebanon
NR
NR
NR
X
Libya
NR
X
NR
NR
Malaysia
X
X
NR
NR
Mauritius
X
NR
NR
NR
Mexico
NR
X
X (5,58)
NR
Montenegro
NR
X
NR
NR
Namibia
NR
X
NR
NR
Peru
X
X
X (59)
NR
Romania
NR
X
NR
X
Serbia
X
X
NR
NR
South Africa
NR
X
X (53,54)
NR
Thailand
X
X
X (60)
X
Tunisia
X
X
NR
NR
Turkey
X
NR
X (61)
X
Lower middle
Armenia
NR
X
NR
NR
Bhutan
NR
NR
NR
X
Cameroon
NR
NR
NR
X
Côte d'Ivoire
X
X
NR
NR
Egypt
NR
NR
X (62,63)
X
El Salvador
NR
X
NR
NR
Georgia
NR
NR
X (64)
X
Ghana
NR
NR
X (65)
X
Guatemala
NR
NR
X (66)
X
Page 5 of 13
Income level, country
OIE survey
Reporting to OIE
Web of Knowledge
Influenza Research
Database
India
NR
X
X (67)
NR
Lesotho
NR
X
NR
NR
Mauritania
NR
NR
X (54)
NR
Mongolia
X
X
X (21,38,68,69)
X
Morocco
NR
X
NR
NR
Nigeria
NR
X
X (70)
NR
Pakistan
NR
NR
X (71)
NR
Papua New Guinea
NR
NR
NR
X
Paraguay
NR
X
NR
NR
Moldova
NR
X
NR
NR
Republic of the Congo
NR
NR
NR
X
Senegal
NR
X
X (54)
NR
Sri Lanka
NR
NR
NR
X
Sudan
NR
X
NR
X
Swaziland
NR
X
NR
NR
Ukraine
NR
NR
X (72)
NR
Vanuatu
NR
X
NR
NR
Vietnam
X
NR
X (73,74)
X
Yemen
X
NR
NR
NR
Zambia
NR
NR
X (75)
NR
Low
Bangladesh
X
X
X (76)
X
Benin
NR
X
NR
X
Cambodia
NR
NR
X (77)
X
Central African Republic
NR
NR
NR
X
Eritrea
NR
X
NR
NR
Ethiopia
NR
X
NR
NR
Guinea
NR
X
NR
NR
Haiti
NR
X
NR
NR
Kenya
NR
NR
X (76)
NR
North Korea
X
NR
NR
NR
Madagascar
NR
X
NR
NR
Mali
NR
NR
X (54)
NR
Mozambique
NR
NR
X (53,54)
NR
Nepal
NR
X
NR
NR
Tanzania
NR
X
NR
NR
Uganda
NR
X
NR
X
Zimbabwe
NR
X
X (53,54)
X
*Reported surveillance by country as per 1) responses to OIE survey confirming surveillance activity; 2) official reports to OIE indicating surveillance
activities, 2008–2012; 3) Web of Knowledge literature indicating surveillance activities during 2008–2013; and 4) information reported to the Influenza
Research Database. Country income levels are based on the 2013 United Nations categorization. OIE, World Organisation for Animal Health; X, ≥1 report
was found in the relevant reporting category; NR, no report. Values in parentheses are references.
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