REVIEW

Poultry food products—a source of avian influenza virus transmission to

humans?

T. C. Harder1, S. Buda2, H. Hengel3, M. Beer1 and T. C. Mettenleiter1

1) The Federal Research Institute for Animal Health, Friedrich-Loeffler-Institut, Greifswald Insel-Riems, 2) Robert-Koch-Institut, Berlin and 3) Institute of Virology,
Department of Medical Microbiology and Hygiene, University Medical Centre, Albert-Ludwigs-University Freiburg, Freiburg, Germany

Abstract

Global human mobility and intercontinental connectivity, expansion of livestock production and encroachment of wildlife habitats by invasive
agricultural land use contribute to shape the complexity of influenza epidemiology. The OneHealth approach integrates these and further
elements into considerations to improve disease control and prevention. Food of animal origin for human consumption is another
integral aspect; if produced from infected livestock such items may act as vehicles of spread of animal pathogens, and, in case of zoonotic
agents, as a potential human health hazard. Notifiable zoonotic avian influenza viruses (AIV) have become entrenched in poultry
populations in several Asian and northern African countries since 2003. Highly pathogenic (HP) AIV (e.g. H5N1) cause extensive poultry
mortality and severe economic losses. HPAIV and low pathogenic AIV (e.g. H7N9) with zoonotic propensities pose risks for human
health. More than 1500 human cases of AIV infection have been reported, mainly from regions with endemically infected poultry. Intense
human exposure to AIV-infected poultry, e.g. during rearing, slaughtering or processing of poultry, is a major risk factor for acquiring
AIV infection. In contrast, human infections through consumption of AIV-contaminated food have not been substantiated. Heating poultry
products according to kitchen standards (core temperatures 70°C, 10 s) rapidly inactivates AIV infectivity and renders fully cooked
products safe. Nevertheless, concerted efforts must ensure that poultry products potentially contaminated with zoonotic AIV do not
reach the food chain. Stringent and sustained OneHealth measures are required to better control and eventually eradicate, HPAIV from
endemic regions.
Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All
rights reserved.

Keywords: Avian, food safety, heat treatment, influenza, OneHealth, transspecies transmission, zoonosis
Article published online: 12 December 2015

Corresponding author: T.C. Harder, The Federal Research Insti-
tute for Animal Health, Friedrich-Loeffler-Institut, Institute of Diag-
nostic Virology, Suedufer 10, Greifswald 17493, Germany
E-mail: timm.harder@fli.bund.de
Introduction
There is a constantly increasing demand to provide food,
including high-quality animal proteins, for an ever-growing hu-
man population [1]. As an ‘entrepreneurial response’ towards
these demands an immense increase in industrialized livestock
production has occurred particularly in the last two decades
[2]. Poultry offers highly economical feed-use efficiency rates
associated with very low carbon costs, which explains the sharp
rise in global poultry production particularly in South East Asia
[3]. Poultry rearing is also very well suited to village-level and
even family-level production, most notably in low-resource
regions. However, altered and intensified poultry production
and trading practices also enhance the risks for acquisition and
spread of infectious diseases not only imposing negative effects
on animal health but also with possible impact on food safety
and human health. Food safety comprises all measures and
facets of producing and handling food items that are dedicated
to prevent illness resulting from consumption [4].
Along with the intensification of poultry production an in-
crease in outbreaks of avian influenza viruses (AIV) in poultry
has occurred [5,6]. Although avian influenza continues to pri-
marily be an issue concerning poultry health, certain AIV strains

Clin Microbiol Infect 2016; 22: 141–146

Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved
http://dx.doi.org/10.1016/j.cmi.2015.11.015
142 Clinical Microbiology and Infection, Volume 22 Number 2, February 2016
show a propensity to also infect mammalian hosts, including
humans. Therefore, AIV-infected poultry flocks may carry
zoonotic risks, and public health awareness towards zoonotic
AIV infections has increased steadily [7]. An increasing rate of
human AIV infection with a lethal outcome has been observed,
notably after 2003. Up to November 2015, WHO has regis-
tered 844 confirmed cases in humans of infection with highly
pathogenic (HP) AIV H5N1 and 681 cases in humans due to
H7N9 AIV showing case fatality ratios of 53% and 40%,
respectively [8,9]. Consequently, concerns were raised about
the threat to humans from poultry viruses, the safety of food
products derived from poultry, and the pandemic potential of
zoonotic AIVs like H5N1 and H7N9.
AIV pathobiology
Avian influenza viruses are members of the influenza A virus
genus in the Orthomyxoviridae family containing eight segments
of single-stranded genomic RNA of negative polarity. Based on
genetic and antigenic differences of their two major membrane
glycoproteins, 16 haemagglutinin (H) and nine neuraminidase
(N) subtypes are currently known in AIV. In their natural hosts,
aquatic wild birds of the orders Anseriformes and Chara-
driiformes, AIV induce acute, in most cases mild and self-
limiting, infections of the epithelium of respiratory and gastro-
intestinal tracts. Infections are usually clinically inconspicuous
[10]. Virus excretion mainly occurs through the oropharyngeal
and cloacal routes, resulting in transmission not only by direct
contact with infected hosts but also indirectly through
contaminated feeding grounds and surface waters [11]. In sur-
face waters, AIV can retain infectivity for more than 6 months
under favourable environmental conditions (low temperature
and salinity, neutral to slightly alkaline pH values), which may
contribute to the sustained endemic transmission of these vi-
ruses in their natural host populations [12,13].
In contrast to galliform poultry, domestic waterfowl are
considered susceptible to most of the AIV subtypes circulating
among aquatic wild birds. Productive infection of chickens and
turkeys often requires adaptation by the virus [14,15]. In gen-
eral, AIV infection in poultry causes only mild, inconspicuous
clinical signs, although a substantial drop in egg production
might ensue. Such AIV infections in poultry are referred to as
low pathogenic (LP) AIV. However, in the case of concurrent
infections with bacterial/parasitic opportunistic pathogens and/
or adverse environmental conditions (e.g. high ambient tem-
peratures) some LPAIV infections can exacerbate and,
depending on poultry species and age of hosts, cause substantial
morbidity and mortality. The widespread LPAIV infections by
subtype H9N2 in turkeys and chickens cause considerable
Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved, CMI, 22, 141–146
CMI
economic losses. LPAIV of subtypes H5 and H7 can sponta-
neously mutate into HPAIV, which cause extensive mortality in
poultry and, often to a much lesser extent, in domestic
waterfowl and wild birds [10]. Hence, all infections of poultry
with H5 or H7 AIV (both LPAIV and HPAIV) are notifiable to
the veterinary authorities. Likewise, the occurrence of HPAIV
in wild birds is notifiable. Notification regulations apply to na-
tional laws; directives 94/2005/EC and 437/2006/EC provide
the legal framework in the European Union regarding all mea-
sures related to combat notifiable AIV. All outbreaks of noti-
fiable AIV have to be reported by the national authorities to the
World Organization for Animal Health (OIE) [16].
In contrast to epithelial infections caused by LPAIV, HPAIV
induce systemic infections affecting the whole organism with
various organs. HPAIV replication causes high titres of infec-
tious virus in internal organs (e.g. liver, heart) and also in muscle
[10,17]. Accordingly, feline and mustelid predators became
infected with HPAIV and diseased when consuming infected
birds [18,19]. Likewise, the reproductive tract is affected during
HPAIV infection [20] and infectious virus is excreted in yolk
(ovary infection) and albumen (oviduct infection) and can also
be found on the egg shell [21]. However, laying activity of
infected poultry ceases rapidly after HPAIV infection and egg
shells from infected layers are often malformed. In addition,
feather cones of HPAIV-infected poultry and wild birds harbour
infectious virus [22]. Although viraemic spread of LPAIV has
also been described [23], these viruses are to a large extent
replication-incompetent outside the gastrointestinal and respi-
ratory tissues. In these cases infectivity titres, e.g. in muscle or
liver tissues, will be very low. Recently, some LPAIV strains of
the H10 subtype have been shown to be able to replicate in
kidneys of infected chickens [24]. It should be noted in this
context that due to the avian anatomy, remnants of kidney and
lung tissues usually remain in poultry carcasses in the course of
industrial, modern slaughtering processes.
AIV as zoonotic agents
Accidental transmission of AIV from infected birds to mammals
occurs sporadically. In rare events, new stable influenza lineages
may evolve from transspecies transmission events as docu-
mented for viral lineages of avian origin circulating in swine,
horse, marine mammals and humans [7]. Since 1959 more than
1500 human AIV infections have been confirmed, with a lethal
outcome in about 48% [25,26]. The majority of these cases
were observed from 2003 onwards and were mainly caused by
the Asian origin HPAIV H5N1 and by an LPAIV of subtype
H7N9 that circulates in China [27,28]. Apart from subtypes H5
and H7 sporadic infections with H6, H9 and H10 viruses of
CMI Harder et al. Avian influenza and poultry food product safety 143

FIG. 1. Mouth-to-beak watering of a

pigeon fledgling at a live poultry
market in Cairo, Egypt—an unusual
human–poultry interface. Given the
often hot climatic conditions young
pigeons require frequent watering
when presented for sale at live
poultry markets in Egypt. As the
birds are too young to effectively
drink enough water themselves (pi-
geon fledglings are used to being fed
a ‘crop milk’ by their parents) ‘assis-
ted’ watering is required. The animal
keeper sucks up a mouthful of water
from a bucket (left) and then installs
the head of a fledgling into his mouth
while forcing open the beak of the
bird between his thumb and fore-
finger (right). Water from his mouth
is then pressed into the crop of the
fledgling. This habit is considered
absolutely common practice.
Although pigeons can be experi-
mentally infected by HPAIV H5N1,
and some natural infections have
been reported (including cases from
Egypt), this species is generally
considered to have a very low sus-
ceptibility to AIV infections [58].
Nevertheless, other (zoonotic)
pathogens may be present.

avian origin have been documented as well [25,26]. So far, all of
these viruses lack sufficient adaptation for effective infection of,
replication in, and excretion from human respiratory tissues
[29]. Therefore, transmission has been ineffective and infre-
quent even in areas where AIV infection is endemic in poultry
resulting in large-scale exposure of the human population.
However, every human infection with a zoonotic influenza A
virus should be reported to WHO in accordance with inter-
national health regulations because of the pandemic potential.
Food safety of poultry carcasses and poultry commodities be-
comes much more relevant compared with other zoonoses
with a comparable burden of disease in human beings [26].
Possible interfaces between infected poultry and humans
that bear risks of AIV transmission have been analysed [30,31].
The highest risks are attributed to contact with infected
poultry, either sick (HPAIV infection, e.g. H5N1) or asymp-
tomatic (LPAIV, e.g. H7N9) [26,32]. Potential transmission
Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved, CMI, 22, 141–146
pathways include inhalation, ingestion, oral or conjunctival
mucosal contacts but the exact modes are incompletely un-
derstood. There may be contacts between poultry and humans
that are not readily envisaged but that are common practice in
those countries where zoonotic AIV are currently endemic, i.e.
Egypt, China, Vietnam and Indonesia (Fig. 1). The majority of
infected humans reported recent visits to live poultry markets
or direct handling of poultry, but direct contact with wild birds
may also pose a risk of infection [33]. Unprotected handling of
infected sick or dead poultry, food preparation from infected
poultry or rearing infected poultry in the household have been
described as behaviours associated with a particularly high risk
[34,35]. High-risk practices include consumption of raw prod-
ucts (e.g. drinking of duck blood or eating uncooked embryo-
nated eggs—as practised in some regions of South East Asia)
obtained from infected poultry. Larger uncertainty exists about
risks of exposure that do not involve physical contact with
144 Clinical Microbiology and Infection, Volume 22 Number 2, February 2016 CMI

poultry, i.e. through contaminated fomites, environment (sur- Conclusions

face waters) or with infected intermediate hosts (cats, pigs)
[31]. Indeed, a substantial number of human cases presented
In conclusion, infectious AIV, in particular highly pathogenic
without known exposure to poultry [26,31,36]. It has to be
biotypes that cause systemic infection in poultry, can be present
mentioned, that no reports are available describing human
in products from infected birds. Viral infectivity titres in these
infection after consumption of properly processed poultry
commodities have been shown to be sufficient to induce pro-
products.
ductive infection in carnivores (mustelids, including ferrets, as
Although clusters of human AIV infections affecting family
well as felids) following ingestion of raw meat and carcasses
members have been reported, these resulted from close-contact
[47,48]. Standardized industrial pasteurization processes, as
nursing of an infected patient and not by effective human-to-
well as proper individual processing and cooking routines, of
human virus transmission, which relies on aerosols [37].
poultry meat and egg products result in complete inactivation of
Consistent with this observation, common exposure to (infec-
viral infectivity [49]. Consequently, human consumption of
ted) poultry was the most likely source of infection in most
properly processed and cooked poultry products is safe. To
human family clusters although human-to-human transmission
date no reports have conclusively linked human infections to
could not always be excluded.
contaminated poultry commodities. Instead, risks for human
infection primarily arise from contact with live or dead infected
Zoonotic AIV in poultry commodities poultry (e.g. through food preparation practices such as
slaughtering, defeathering, cutting/cleaning of raw meat,
removing and/or cleaning internal organs) and its contaminated
International trading rules have been formulated by the OIE to
environment. Such risks are increased in societies that prefer
ensure safe trade of poultry products [16]. Trading of poultry is
products from freshly slaughtered poultry, which is usually is
permitted from regions (countries, zones or production com-
associated with village or family production systems and live
partments) that have been assigned a status of freedom from
poultry market trading in countries where AIV are endemic in
notifiable AIV infections. Continuous surveillance of poultry
poultry. Reducing these contacts, e.g. by closing live poultry
populations for notifiable AIV is required to demonstrate this
markets—as was effectively practised during waves of human
status for a country or region therein over time. In case of
infections with AIV H7N9 in China [50,51]—aids in minimizing
outbreaks of notifiable AIV extensive restriction measures are
risks of human AIV infections. Although the principal mode of
implemented to control the outbreak and eradicate the infec-
transmission of zoonotic AIV in the endemically infected re-
tion. This includes (1) culling of the poultry population of
gions is through transport of infected poultry or their products,
affected flocks, holdings or regions and (2) temporary cessation
the specific modes of transspecies transmission to humans are
of trade. Specific national animal disease regulations following
still ill-defined. OneHealth management tools such as hazard
the OIE standards are in place to ensure that notifiable animal
analysis of critical control points are expected to aid in iden-
diseases including AIV are appropriately dealt with.
tifying key points of contact at the poultry–human interface.
Based on the pathobiology of zoonotic AIV infections, in
Detailed algorithms depicting the flow of poultry production
particular HPAIV, sufficient viral infectivity to cause interspecies
have been presented for Vietnam [52]. This analysis identified
transmissions can be present in poultry commodities from
two key critical control points that, apart from direct contact
infected birds. Excellent reviews on the presence of AIV in
with poultry dying from HPAIV infection [35], were pivotal in
poultry commodities have recently been published [38,39]. The
mediating virus transmission to humans: slaughtering and
undetected presence of zoonotic AIV in unprocessed poultry
preparation of carcasses/meat of infected poultry. Preventive
products is a general risk for further spread among poultry
measures at these critical control points therefore should
[40,41] and for exposure of humans.
include both technical and personal protective equipment that
A series of investigations targeted inactivation kinetics of
limit the generation/spread of (e.g. by aerosolization or droplet
HPAIV and LPAIV in various matrices and environmental con-
formation), and restrict contacts with, infectious material dur-
ditions including meat and egg products. Heat inactivation was
ing these processes. Education and adequate risk communica-
consistently found to be highly effective in inactivating infectivity
tion to the populations at risk is another important intervention
within a few seconds at temperatures of at least 70°C [42]. This
factor of OneHealth relevance [53]. Yet, despite at least basic
indicates that properly cooked poultry meat and eggs do not
awareness of the risks associated with poor biosecurity and
pose a risk of infection [43]. Also, the standard industrial
hygiene while handling, slaughtering or defeathering potentially
pasteurization protocols for a variety of egg products were
infected poultry, many obstacles hamper the implementation of
found to sufficiently reduce risks of AIV transmission [44–46].
Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved, CMI, 22, 141–146
CMI
more effective prevention provisions; such impediments are
most often related to economic and sociocultural pressures
[54,55].
In addition, an improved understanding of the modes of AIV
transmission to humans is required. It is important to realize
that during each human infection with AIV these viruses gain a
chance to adapt and launch potentially sustainable human-to-
human transmission chains [56]. One recent example was the
unexpected upsurge in human cases with HPAIV H5N1 in
Egypt, which prompted a high-level mission of six organizations
(WHO, FAO, OIE, US-CDC, US-NAMRU-3, UNICEF) to
assess the H5N1 situation in the country [57]. These scenarios
clearly demand continuous, intensive OneHealth approaches to
further guarantee farm-to-table food security, to prevent AIV-
contaminated products reaching the food chain, and to mini-
mize the risks of human exposure to zoonotic AIV.
Acknowledgements
The authors are grateful to Walter Haas for critically reading
the manuscript.
Transparency declaration
The authors declare that they have no conflicts of interest.
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