Clinical Infectious Diseases
972 • CID 2019:68 (15 March) • Bui et al
Bioaerosol Sampling to Detect Avian Infuenza Virus in
Hanoi’s Largest Live Poultry Market
Vuong N. Bui,
1
Tham T. Nguyen,
2
Hung Nguyen-Viet,
3,4
Anh N. Bui,
1
Katie A. McCallion,
5
Hu Suk Lee,
3
Son T. Than,
1
Kristen K. Coleman,
2
and
Gregory C. Gray
2,6,7
1
Virology Department, National Institute of Veterinary Research, Hanoi, Vietnam;
2
Program in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore;
3
International Livestock
Research Institute, Hanoi, Vietnam, and
4
Center for Public Health and Ecosystem Research, Hanoi University of Public Health, Vietnam;
5
College of Veterinary Medicine, North Carolina State
University, Raleigh, North Carolina, and
6
Division of Infectious Diseases, Global Health Institute, and Nicholas School of the Environment, Duke University, Durham, North Carolina; and
7
Global
Health Research Center, Duke-Kunshan University, China
Background. Newly emergent and virulent strains of H7N9 avian infuenza virus are rapidly spreading in China and threaten to
invade Vietnam. We sought to introduce aerosol sampling for avian infuenza viruses in Vietnam.
Methods. During October 2017, National Institute for Occupational Safety and Health 2-stage aerosol samplers were assembled
on a tripod and run for 4 hours. Concomitantly, up to 20 oropharyngeal (OP) swab samples were collected from chickens and ducks
distanced at 0.2–1.5 m from each sampler.
Results. Te 3 weeks of sampling yielded 30 aerosol samples that were 90% positive for infuenza A, by quantitative reverse-tran-
scription polymerase chain reaction, and 116 OP swab sample pools (5 samples per pool) that were 47% positive. Egg cultures
yielded 1 infuenza A virus (not H5 or H7) from aerosol and 25 infuenza A viruses from OP swab sample pools (5 were H5 positive).
Te association between positive sample types (over time and position) was strong, with 91.7% of positive OP pooled swab samples
confrmed by positive aerosol samples and 81% of infuenza A positive aerosol samples confrmed by positive OP swab samples.
Conclusions. We posit that aerosol sampling might be used for early warning screening of poultry markets for novel infuenza
virus detection, such as H7N9. Markets with positive aerosol samples might be followed up with more focused individual bird or
cage swabbing, and back-tracing could be performed later to locate specifc farms harboring novel virus. Culling birds in such farms
could reduce highly pathogenic avian infuenza virus spread among poultry and humans.
Keywords. avian infuenza; infuenza A virus; Vietnam; poultry; epidemiology.
In recent years, avian influenza virus outbreaks have caused a
massive number of poultry deaths, resulting in the destruction
of poultry markets and farms in multiple world regions [1–4].
Monitoring and controlling such outbreaks among poultry
is important for public safety, because human infections can
occur through direct contact with infected poultry and their
surrounding environments. For example, H5N1 avian influenza
virus outbreaks resulted in 26 human infections and 14 deaths
in Cambodia in 2013, and 173 human infections and 53 deaths
in Egypt from 2014 to 2015 [5]. More recently, from October
2016 to 28 March 2018, the H7N9 avian influenza virus out-
break resulted in 822 confirmed human infections and at least
307 human deaths [6]. Furthermore, the H7N9 virus has spread
to western China (Guangxi Province), and a highly pathogenic
strain has emerged [7], which scientists anticipate will soon
breach the China-Vietnam border through formal and informal
live poultry trade [8].
To mitigate the further spread of H7N9, Vietnam’s Ministry
of Health’s General Department of Preventive Medicine has or-
dered public safety dispatchers to halt the smuggling of poultry
and poultry products from the Chinese border into Vietnam.
Health workers in bordering provinces have also been trained in
the surveillance, diagnostic testing, and treatment for potential
outbreaks [9]. However, despite diligent preparations, Vietnam’s
surveillance system is spotty, lacking a quick and efective tool
to detect the incursion of viruses in large-scale poultry markets.
In a pilot efort to enhance avian infuenza virus surveil-
lance, our team employed a bioaerosol sampling method using
National Institute for Occupational Safety and Health (NIOSH)
2-stage aerosol samplers [10–12] to monitor for and capture live
avian infuenza H5N1 and H7N9 viruses from the largest live
poultry market in Hanoi, Vietnam.
MATERIALS AND METHODS
Study Site
Our study took place during the first 3 weeks of October 2017 at
Ha Vi Market (Supplementary Figure 1), the largest live whole-
sale poultry market in Hanoi, Vietnam. It is estimated that
MAJOR ARTICLE
© The Author(s) 2018. Published by Oxford University Press for the Infectious Diseases Society
of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com.
DOI: 10.1093/cid/ciy583
Received 23 April 2018; editorial decision 29 June 2018; accepted 11 August 2018; published
online August 31, 2018.
Correspondence: G. C. Gray, Division of Infectious Diseases, Duke University Medical Center,
Duke University, Box 102359, Durham, NC 27710 (gregory.gray@duke.edu).
Clinical Infectious Diseases
®
2019;68(6):972–5