Editorial Commentary: This Little Piggy Went to Market—but Perhaps Should Have Stayed Home
This Little Piggy Went to Market-but Perhaps Should Have Stayed Home
Richard J. Webby 0
0 Department of Infectious Diseases, St Jude Children's Research Hospital , Memphis, Tennessee
influenza; zoonotic; animal markets
Influenza A is a zoonotic disease.
Although some causative viruses have
become adapted to humans and circulate
exclusively in this host, the animal
reservoirs are the source of all past and future
pandemic strains. With this knowledge,
there has been decades of research toward
identifying the interfaces where infected
animals and humans are most likely to
interact. A particular target of these
studies has been live bird markets,
particularly in Asia. While the importance of these
markets had been previously recognized
, the H5N1 outbreak in Hong Kong
in 1997, where 6 of 18 persons known
to be infected with the virus died,
refocused much of influenza’s public health
attention . Live bird markets provide
a prime environment to support the
evolution of influenza A viruses and promote
human infection. Not only are different
hosts of influenza—including humans—
each with their own variants of the virus,
brought together in unnatural proximity,
but as fresh animals are introduced to
replenish stocks, new susceptible hosts are
made available, allowing the virus to
spread and be maintained for prolonged
periods. The importance of live bird
markets in the ecology of influenza was again
highlighted in 2013 when human H7N9
infections were detected in China .
The correlation between the closing of
the market systems and the drop-off in
human cases suggested markets as the
likely source of infection.
Although mammalian species have
been present in some of the markets
studied, the majority of influenza work has
centered on the role of the avian species.
In this issue of Clinical Infectious
Diseases, Choi and colleagues have provided
convincing evidence that animal markets
that sell swine present another active
interface in which infected animals and
humans interact and where zoonotic
infections occur . Surprising to many will be
the fact that these markets are located
not in Asia, but in the United States. In
what is a textbook example of
collaboration between academia and veterinary
and public health, this team of
investigators undertook a 12-week surveillance
program in 2 mixed-species markets in
the state of Minnesota targeting swine,
environmental surfaces, and employees.
The 2 markets were selected based on
epidemiologic evidence that suggested them
as possible sources for prior zoonotic
Although a number of interesting
observations were made and detailed in the
manuscript, one striking finding was the
surprisingly high level of influenza virus
detected in market employees. Eleven of
the 17 employees tested positive at least
once for the presence of influenza virus
RNA during the 12-week period.
Although half of these positive samples
were unsubtypable due to viral load
issues, 4 were confirmed to be H3N2
viruses of swine origin, with the remaining
7 being seasonal H3N2 influenza viruses.
The relatively high detection of H3N2
viruses of swine origin in the employees is a
challenge to interpret. Real-time reverse
transcription polymerase chain reaction
(PCR) cycle threshold values were all high,
and it is possible that detections
represented true viral infection or, alternatively,
fomite contamination of the nasal cavity.
Influenza viruses were detected in pigs,
air samples, pen railings, and other
environmental surfaces in the markets, and
there was a marked lack of clinical
symptoms reported, indicating that the latter is
a real possibility. Regardless, the fact that
virus genetic material was detected in
nasal cavities demonstrates ample
exposure and, at minimum, a threat of
infection. Unfortunately, the high degree of
antigenic similarity between many of
the swine and human influenza viruses
circulating in the United States, and in
many parts of the world, limits the
usefulness of serology in interpreting the PCR
results. Indeed, most of the employees
had baseline serologic reactivity to the
swine viruses, including 67% with
immunity to the H3N2 swine viruses detected.
This alone could account for the low
levels of clinical symptoms reported.
Somewhat fortuitously for the study, but not
the patient, a 12-year-old boy developed
respiratory illness 3 days after visiting
one of the markets. Follow-up studies
showed that he was infected with a virus
with gene segments near-identical to
those detected in swine in the same
location, direct evidence of market-to-human
Studies such as this one are not simple
to conduct, with a number of
professional, ethical, and trust issues to overcome.
They are, however, critical to further our
understanding of zoonotic influenza and
the factors that favor it, and to fuel
subsequent laboratory studies to identify the
underlying virologic features of
interspecies transmission. As such, the authors
are to be congratulated on an important,
invaluable, and well-conducted study.
The amount of education, preparation,
and consultation that went into this
study must have been substantial.
On another level, this study again
brings into question the wisdom of live
animal markets. There is ample evidence to
support a human health threat from live
birds in these markets, and now
mammalian hosts as well. While there is a clear
cultural demand for their products, there
is also an undisputable risk. There is
currently much discussion on
influenzarelated laboratory biosafety issues. Markets
such as the one described in this study
represent a far greater threat; changes must be
made to how they operate. Whether it is
manipulations to airflow, animal
husbandry, sanitary practices, or other novel
solutions, studies to assess the impact of
intervention strategies in real-world
settings are needed. Since 1997, Hong Kong
authorities have implemented a number
of programs that have reduced the diversity
and overall viral burden within their
poultry markets (see, eg, ), providing proof
that it can be done. In each case, these
decisions were based on solid, but not
necessarily highly fundable, scientific
studies. The scope of the problem is
large, but the hurdles not unsurmountable.
Studies such as that by Choi et al are the
perfect place to start.
Potential conflict of interest. Author certifies
no potential conflicts of interest.
The author has submitted the ICMJE Form
for Disclosure of Potential Conflicts of Interest.
Conflicts that the editors consider relevant to the
content of the manuscript have been disclosed.
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