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A One Health approach to antimicrobial resistance surveillance:
is there a business case for it?
Kevin Queenan a,
*, Barbara Häsler a,b
, Jonathan Rushton a
a Veterinary Epidemiology, Economics and Public Health Group, Department of Production and Population Health, Royal Veterinary College,
Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK
b
Leverhulme Centre for Integrative Research on Agriculture and Health (LCIRAH), Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield,
Hertfordshire AL9 7TA, UK
A R T I C L E I N F O
Article history:
Received 19 February 2016
Accepted 18 June 2016
Keywords:
Antimicrobial resistance
AMR
Surveillance
One Health
Business case
Economics
A B S T R A C T
Antimicrobial resistance is a global problem of complex epidemiology, suited to a broad, integrated One
Health approach. Resistant organisms exist in humans, animals, food and the environment, and the main
driver of this resistance is antimicrobial usage. A One Health conceptual framework for surveillance is
presented to include all of these aspects. Global and European (regional and national) surveillance systems
are described, highlighting shortcomings compared with the framework. Policy decisions rely on eco-
nomic and scientific evidence, so the business case for a fully integrated system is presented. The costs
of integrated surveillance are offset by the costs of unchecked resistance and the benefits arising from
interventions and outcomes. Current estimates focus on costs and benefits of human health outcomes.
A One Health assessment includes wider societal costs of lost labour, changes in health-seeking behaviour,
impacts on animal health and welfare, higher costs of animal-origin food production, and reduced con-
sumer confidence in safety and international trade of such food. Benefits of surveillance may take years
to realise and are dependent on effective and accepted interventions. Benefits, including the less tangi-
ble, such as improved synergies and efficiencies in service delivery and more timely and accurate risk
identification, should also be recognised. By including these less tangible benefits to society, animal welfare,
ecosystem health and resilience, together with the savings and efficiencies through shared resources and
social capital-building, a stronger business case for a One Health approach to surveillance can be made.
© 2016 Elsevier B.V. and International Society of Chemotherapy. All rights reserved.
1. Introduction and background
In 2001, the World Health Organization (WHO) described anti-
microbial resistance (AMR)1
as a global problem requiring a global
response [1], but until recently it has failed to gain the urgent at-
tention it deserves. Economic evidence is used as a tool to prioritise
policy decisions and it has been argued that previous estimates of
the health cost of AMR have been too negligible [2] and they have
failed to consider the wider impacts on health care [3]. However,
recently more alarming estimates of AMR have appeared in the lit-
erature. The European Commission claimed that costs attributed to
resistant bacterial infections amounted to €1.5 billion annually [4].
Healthcare systems in the USA estimate the additional cost of
antimicrobial-resistant infections to be US$20 billion a year and pro-
ductivity losses to be US$35 billion a year [5]. The UK government-
commissioned ‘Review of antimicrobial resistance’ estimated that drug-
resistant infections could cause 10 million human deaths annually
by 2050, with total costs by this date of US$100 trillion in lost output
[6].
Disease surveillance provides evidence for informed decisions
on interventions, and AMR surveillance is no exception [7,8]. Sur-
veillance of AMR is critical for impact evaluation of, for example,
interventions that change guidelines on antimicrobial usage or in-
fection control [9]. Moreover, it provides information on AMR
emergence and occurrence relevant for the public, patients, health-
care providers, governmental agencies and researchers [7].
Despite the WHO calling for local, national and global AMR sur-
veillance systems to be established [8], gaps in surveillance remain,
primarily through lack of capacity and integration [10]. The US Na-
tional Action Plan proposed the strengthening of a ‘One Health’
national surveillance system (for humans, animals and the envi-
ronment) with improved international collaboration and capacity
[11]. One Health, however, also refers to a broad, systems-based ap-
proach to complex problems [12]. It is therefore suited to AMR
surveillance because it considers the underlying structural factors
* Corresponding author. Veterinary Epidemiology, Economics and Public Health
Group, Department of Production and Population Health, Royal Veterinary College,
Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK. Fax: +44 0
1707 666333.
E-mail address: kqueenan3@rvc.ac.uk (K. Queenan).
1
Although by definition AMR refers to resistance of all microbes including bac-
teria, viruses, parasites and fungi, this paper and the majority of the literature use
the term with a bias towards bacterial resistance.
http://dx.doi.org/10.1016/j.ijantimicag.2016.06.014
0924-8579/© 2016 Elsevier B.V. and International Society of Chemotherapy. All rights reserved.
International Journal of Antimicrobial Agents 48 (2016) 422–427
Contents lists available at ScienceDirect
International Journal of Antimicrobial Agents
journal homepage: www.elsevier.com/locate/ijantimicag
that influence AMR, including the sociopolitical, material, biolog-
ical and economic factors [13]. A One Health approach also includes
an analysis of the context and institutional environment in which
decisions are made across all levels of society [14].
In recognition of the above, this paper proposes a framework to
promote a One Health surveillance system for AMR. Resistance is
a global concern, with no regard for national borders, degree of
healthcare sophistication or national gross domestic product (GDP)
[15]. Despite this, not all regions of the world have promoted in-
tegrated AMR surveillance systems. To assess the level of integration,
strengths, challenges and weakness, literature on the current global,
regional (European) and selected European national surveillance
systems is reviewed and positioned against the proposed frame-
work. Whilst the economic benefits for a One Health approach to
zoonotic infectious disease surveillance have been published else-
where [16–19], this paper builds a business case for a One Health
approach to AMR surveillance.
2. Why a One Health approach and fully integrated
surveillance system?
The discussion of AMR is often focussed on human health out-
comes. However, a broader consideration of the impacts on animal
and environmental health is essential. Prescott discussed the complex
epidemiology of AMR and stated that ‘resistance anywhere is re-
sistance everywhere’ [20]. AMR is described as an ecological problem
by Radhouani et al [21], and as ‘a highly multifaceted topic at the
interface of human, animal and plant health, food hygiene and en-
vironmental science’ by Butaye et al [22].
Antimicrobial usage (more specifically antibiotics)2
and the re-
sultant selective pressure have been recognised as the main drivers
for AMR [23,24]. It is therefore essential to link antimicrobial usage
data with AMR surveillance data when considering methods for AMR
containment. The combined surveillance would also facilitate moni-
toring of the impact of interventions aimed to improve antibiotic
stewardship and reduce consumption [9]. The widespread use of
biocidal soaps and gels versus simple soap handwashing and the
benefits of potentially reducing the spread of institutional infec-
tions versus contributing to AMR are other areas for consideration
[25].
Rushton stated that antimicrobials should be seen as a common
good [14]. In light of this, human behaviour and attitudes around
antibiotic prescribing and use should be considered both in human
and veterinary medicine. Decisions around antimicrobial usage in
livestock should consider the trade-offs that occur between restor-
ing animal health and productivity, provision of animal welfare and
impacts on livelihoods, hunger and poverty alleviation versus the
risk of driving resistance [14]. Prescribing decisions of companion
animal veterinarians are also influenced by affordability, ease of ad-
ministration and perceived compliance [26]. The environmental
impact of the management of human effluent, waste from live-
stock and aquaculture facilities and from manufacturers of
pharmaceuticals is recognised as a potential hotspot for AMR [27].
These aspects are yet more evidence that a broad, contextual or
institutional analysis is required when considering the use or misuse
of antimicrobials [14]. A systems-based approach to surveillance will
better identify critical control points thereby improving effective-
ness and economic efficiency.
3. One Health framework for antimicrobial resistance
surveillance
A conceptual framework for a One Health approach to AMR sur-
veillance is proposed here and is illustrated in Fig. 1. It centralises
and integrates surveillance both of antibiotic usage or consump-
tion for humans and animals with AMR data from humans, animals,
food and the environment.
Consumption data in humans are gathered in hospital and com-
munity settings, whilst in animals they are gathered at the species
level, i.e. food-producing animals (including fish), companion animals
and wildlife. AMR surveillance in humans includes invasive sam-
pling of clinical cases from hospital and community care settings
as well as non-invasive sampling of commensals. In food-producing
animals, isolates are accessed from clinical cases and commensals
from healthy animals (available at slaughter). Similarly, samples of
clinical cases in companion animals and wildlife are easily ac-
cessed through veterinarians, although commensals from both
groups, especially wildlife, may be less feasible. Surveillance of AMR
in organisms isolated from food includes food originating from
2
In the context of usage, the literature’s focus has been on antibiotics and the
impact on resistance in bacteria.
Fig. 1. An interconnected and integrated One Health surveillance framework that puts at its centre antimicrobial resistance and antimicrobial consumption.
423K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
animals and plants (zoonotic pathogen surveillance from the former
and commensals from both). Environmental surveillance includes
samples from water sources and soil.
Data collected within the various categories require an inte-
grated analysis, facilitated by teams with experience across the
sectors. Similarly, interpretation of the analysis requires teams of
sectoral experts who also possess intersectoral knowledge and un-
derstanding and the collaborative skills to work with those from
other sectors, including social scientists and behaviour change
experts. This is to ensure a One Health approach to developing the
subsequent recommendations.
A centralised programme is required to set standards for data
collection, which is critical at all levels for ease of analysis and in-
terpretation. This will also improve communication and networking
between disciplines and sectors through shared meetings, discus-
sions and report editing.
Centralised leadership and budgeting will be responsible for sup-
porting and enabling peripheral capacity and compliance. However,
this ideal, multidimensional, integrated surveillance may be diffi-
cult to achieve across all categories given the high level of capacity
and logistics required and the commonly found barriers between
siloed institutions. A tiered approach to integration may assist in
building capacity. Within each tier, globally recognised tech-
niques and standards must be adopted and adhered to. The initial
tier would involve relatively standard collection, sharing and anal-
ysis of data and therefore involve less integrated interpretation. The
progression into the higher tiers would involve broadening data col-
lection sources (from Fig. 1). This would require a shift in institutional
mindsets to support the increasing degrees of co-operation and in-
tegration required to facilitate the analysis and interpretation of
results and evolution of joint recommendations.
4. A review of current surveillance systems, from global to
local
A review of the current global and European (regional and na-
tional) surveillance systems was conducted to identify degrees of
integration, with attention to AMR and usage data, sectoral inte-
gration, and which species and which food types and environmental
elements were included in sampling.
4.1. Global systems
The 2008 WHO Advisory Group on Integrated Surveillance of An-
timicrobial Resistance (AGISAR) has 31 internationally renowned
expert advisors including representatives from the World
Organisation for Animal Health (OIE) and the Food and Agricul-
ture Organization (FAO). Their aims include developing standardised
sampling techniques and methodology, providing expert advice, pro-
moting information sharing and supporting capacity-building for
AMR surveillance and antimicrobial usage in member states.
The Global Foodborne Infections Network (GFN) has public health,
veterinary and food-sector professionals, all working towards a global
integrated AMR surveillance system.
CODEX Alimentarius (commissioned by the WHO and FAO) in-
cludes a task force to integrate AMR surveillance in humans with
that in food-producing animals, crops and food.
WHONET is a WHO initiative to support harmonisation of global
surveillance data by providing free software and training to labo-
ratories in over 100 countries within all six WHO regions. The
software facilitates standardised data collection and analysis and
also informal sharing and networking.
The Transatlantic Taskforce on Antimicrobial Resistance (TATFAR)
was established in 2009 as a collaboration between the USA and
the European Union (EU). It aims to promote appropriate use of
antimicrobials in human and veterinary medicine, to prevent re-
sistant infections in hospital and communities and to improve
development of new antimicrobials.
The Joint Programming Initiative on Antimicrobial Resistance
(JPIAMR) is a research group that co-ordinates global research in
AMR. Their One Health research agenda includes AMR in humans,
animals and the environment.
4.2. Regional (European) systems
The European Centre for Disease Prevention and Control (ECDC)
conducts surveillance for AMR and antibiotic consumption in human
health through several networks.
• The European Antimicrobial Resistance Surveillance Network
(EARS-Net) provides guidance to members on data collection,
management, analysis and validation. It collates data from over
900 public health laboratories, which process samples from clin-
ical cases in over 1400 hospitals in 30 EU/European Economic
Area (EEA) countries.
• The European Surveillance of Antimicrobial Consumption
Network (ESAC-Net) collates data on systemic use of antibiot-
ics, antifungals and antivirals in hospital and community sectors
from 32 EU/EEA countries.
• The European Food and Waterborne Diseases and Zoonoses
Network (FWD-Net) is responsible for surveillance of human
pathogens from water, food or animal contact. The data con-
tribute to the European Food Safety Agency (EFSA) and ECDC
annual summary report.
• The Healthcare Associated Infection Network (HAI-Net) co-
ordinates AMR surveillance and antimicrobial use in acute
(intensive care) and long-term care facilities and the surveil-
lance of surgical site infections.
Surveillance of AMR in food-producing animals and food prod-
ucts, as well as veterinary antibiotic consumption, is covered by the
following:
• The European Centre for the Study of Animal Health (CEESA) col-
lects standardised AMR data for a central laboratory, from healthy
animals at slaughter and clinically ill food-producing and com-
panion animals.
• The European Surveillance of Veterinary Antimicrobial Con-
sumption (ESVAC) aims to collect harmonised data on the sales
of veterinary antimicrobials (from wholesalers, veterinarians and
pharmacies) to enable comparison with human consumption
data. Its fourth annual report [28] included data from ca. 95%
of food-producing animals in 26 EU/EEA countries.
• The EFSA collates AMR data within its surveillance of zoonoses
and disease outbreaks from food and food-producing animals.
It supports EU members, providing guidelines on standardising
sampling and processing, so as to harmonise data for analysis.
It produces an annual summary report in conjunction with the
ECDC.
In addition, the ECDC facilitates collaboration of surveillance
groups with the European Committee on Antimicrobial Suscepti-
bility Testing (EUCAST) and the European Society of Clinical
Microbiology and Infectious Diseases (ESCMID). ESCMID has been
active for over 25 years, with a wide range of study groups, some
concerned with specific disease agents and others covering anti-
microbial policy (ESGAP), AMR surveillance (ESGARS) and veterinary
microbiology (ESGVM).
In 2012, building on the success of the ECDC programmes, EARS-
Net was expanded and the Central Asia and European Surveillance
of Antimicrobial Resistance (CAESAR) network was established.
424 K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
4.3. National systems
The WHO’s global report on surveillance of AMR [10] is based
on data from the 129 contributing member states. The report high-
lighted individual national systems that attempt to integrate
surveillance in humans, food-producing animals and food
(Table 1).
Several national systems within EU states have been guided
towards integration through the direction of the European region-
al systems as mentioned in the previous section. Longstanding
examples include the following:
(i) The Danish Integrated Antimicrobial Resistance Monitoring
and Research Program (DANMAP) was established in 1995 as
a collaborative programme between the Ministry of Health
and the Ministry of Food, Agriculture and Fisheries. DANMAP
has implemented a ‘farm to fork to sickbed’ approach to sur-
veillance [29] to include the whole supply chain. Sampling
includes human and animal clinical cases, healthy animals
(randomly at slaughter) and locally produced and imported
meat products at wholesale and retail outlets. Consumption
data are collected from hospitals, primary healthcare centres
and pharmacies. Veterinary medicine usage is registered at
a species level [food-producing animals (including fish) and
companion animals] by veterinarians, pharmacies and feed
mills.
(ii) The Swedish Strategic Programme Against Antibiotic Resis-
tance (STRAMA), founded in 1995, aims to preserve
antimicrobial agent effectiveness in public health. The Swedish
Veterinary Antimicrobial Resistance Monitoring Programme
(SVARM) was established in 2000. STRAMA has produced an
annual report (SWEDRES) on antibiotic use and resistance in
humans since 2001, whilst SVARM’s annual report covered
AMR surveillance in zoonotic bacteria, specific animal patho-
gens, commensal enteric bacteria and bacteria from food of
animal origin. Since 2011, a combined, integrated SWEDRES/
SVARM annual report has been published, demonstrating
intersectoral collaboration.
(iii) The Netherlands has, since 2003, produced NethMap, an
annual report on AMR and antibiotic consumption trends in
humans. MARAN, the veterinary surveillance system, has done
the same for food-producing animals and also includes
isolates from vegetables, fruits and herbs. Since 2012,
a single, combined (NethMap-MARAN) report has been
published.
5. Challenges and shortcomings, recent developments and
future improvements
The review demonstrates evidence of broader sampling, inte-
gration and shared analysis, however thus far no fully integrated
and standardised surveillance system for AMR and antimicrobial
usage, which functions both locally and globally, exists. A lack of
data quantity and quality persists, the latter affected by a lack
of standardisation [30]. There is still insufficient comparable data
of AMR in humans and livestock to develop global mapping of re-
sistance and to allow accurate comparisons between humans, various
livestock species, industries, countries and regions [31].
In 2012, the WHO published results of a survey of existing sur-
veillance networks [32]; 5 international and 22 national networks
responded. Only 30% had a nationally co-ordinated body, whilst <40%
had formal quality assurance requirements and antimicrobial usage
data were generally absent. In the WHO’s global report on surveil-
lance of AMR [10], there was no formal consensus on methodology
and data collection amongst the 129 contributing member states.
At the European level, although EARS-Net advises and encourages
standardisation using EUCAST guidelines, only 64% of the partici-
pating laboratories do so [23]. Global systems are reliant on data
collected nationally. Therefore, standards within data collection need
to be applied at source to allow meaningful interpretation at all
levels, which will require significant investment in developing ca-
pacity. Therefore, in the next section we discuss a business case for
a One Health approach to AMR surveillance.
6. The business case for a One Health approach to
antimicrobial resistance surveillance
Whilst Babo Martins et al provided a framework for a broad eco-
nomic assessment of integrated zoonotic disease surveillance in a
One Health context [19], publications showing direct measureable
impacts of AMR surveillance and interventions from a One Health
perspective were not found. Similarities exist between the busi-
ness case for AMR surveillance and of emerging zoonotic infectious
diseases. In both cases their unpredictable nature makes econom-
ic evaluation dependent on assumptions and/or predictive modelling,
which are often subject to considerable uncertainty. Appreciating
the broad complexity and interconnectivity of human, animal and
environmental outcomes, a One Health, systems-thinking ap-
proach is needed to measure the benefits of investment in integrated
surveillance. Evaluation of economic and empirical scientific aspects
must be blended with an appreciation of the social, cultural and
Table 1
Antimicrobial resistance surveillance systems [10].
Surveillance system, country Surveillance of resistant bacteria from: Bacterial species included
Healthy
animals
Diseased
animals
Food Healthy
humans
Diseased
humans
Salmonella Campylobacter Escherichia
coli
Enterococci Animal
pathogens
CIPARS, Canada X X X X X X X X
DANMAP, Denmark X X X X X X X X X X
FINRES-Vet, Finland X X X X X X X X X
GermVet, Germany X X X X X
ITAVARM, Italy X X X X X X X X
JVARM, Japan X X X X X
NARMS, USA X X X X X X X X
NethMap/MARAN, The Netherlands X X X X X X X X
NORM/NORM-VET, Norway X X X X X X X X X
ONERBA, France X X X X X X X X X
SWEDRES/SVARM, Sweden X X X X X X X X X
CIPARS, Canadian Integrated Program for Antimicrobial Resistance Surveillance; DANMAP, Danish Integrated Antimicrobial Resistance Monitoring and Research Program;
FINRES-Vet, Finnish Veterinary Antimicrobial Resistance Monitoring and Consumption of Antimicrobial Agents; GermVet, German National Antibiotic Resistance Monitor-
ing; ITAVARM, Italian Veterinary Antimicrobial. Resistance Monitoring; JVARM, Japanese Veterinary Antimicrobial Resistance Monitoring System; NARMS, National Antimicrobial
Resistance Monitoring System; MARAN, Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in The Netherlands; ONERBA, Observatoire National de
l’Épidémiologie de la Résistance Bactérienne aux Antibiotiques; SVARM, Swedish Veterinary Antimicrobial Resistance Monitoring Programme.
425K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
ecological aspects [33]; the less tangible and non-monetary out-
comes should be considered in addition to the monetary. These less
tangible benefits include knowledge creation, social and intellec-
tual capital, reduced anxiety, political reassurance and technical
capacity-building. Whilst these are not always easily quantifiable,
they should be considered none the less [19].
Table 2 summarises the costs and benefits envisaged from in-
tegrating surveillance of AMR to a One Health level and also the costs
and benefits of the integrated interventions arising from the One
Health surveillance.
Although costs are incurred in the setup of or conversion into
a One Health system, savings are expected from the effects of shared
and more efficient use of resources, shared running costs and im-
proved outcomes. Using the H5N1 (highly pathogenic avian
influenza) campaign as an example, the World Bank estimated cost
savings of 10–30% from joint investment and 20–40% in costs of
ongoing surveillance through shared staff and facilities. Further
savings in training and research are estimated at 5–10% [34].
Surveillance benefits primarily relate to those arising from the
interventions it spawns. Interventions are often delayed whilst suf-
ficient data are collected and analysed. Benefits may not be immediate
(e.g. the impact on public health outcomes from reduced antimi-
crobial use) and may also be confounded by several factors over time
[35]. Global travel is an example; despite Denmark’s attempts to
control resistance in Campylobacter, 37% of campylobacteriosis cases
in humans were related to international travel, with a higher pro-
portion of these being resistant compared with domestic cases [29].
Positive knock-on effects also need to be recognised. Den-
mark’s integration of antimicrobial consumption data with resistance
data identified specific links, resulting in improved public aware-
ness and government policy [36], which included a ban on the use
of certain antibiotics in livestock and restrictions on veterinarians’
profits from antibiotic sales [37]. In addition, a voluntary ban against
using cephalosporins and fluoroquinolones in food-producing
animals followed. As a result, food-producing animals in Denmark
consume 80% less antimicrobials per kg of meat produced than those
in the USA [37].
A greater understanding is required of the wider implications
and costs of AMR on society. Implications include changes in health-
seeking behaviour, e.g. avoiding invasive procedures because of the
(perceived) risk of untreatable infections [2], increased hospital in-
fection control measures, litigation, and reduced international travel
and trade [38]. Furthermore, reports on the costs of unchecked AMR
fail to consider the impact on the food-producing animal sector and
the effect on livestock-dependent communities and national econo-
mies. The costs of untreatable livestock diseases, increased biosecurity
costs and the costs of lost consumer confidence in the safety of food
of animal origin as well as animal welfare issues need to be included.
7. Discussion
Recent calls to improve the integration of AMR and consump-
tion surveillance are welcomed. This complex, interconnected
problem with negative externalities will require international
intersectoral collaboration. It therefore favours the application of
a One Health approach to the surveillance systems, the interven-
tions and the evaluation of outcomes.
The European national surveillance systems reviewed in this
paper all fall short of the One Health framework presented above,
with none mentioning the environment or wildlife. DANMAP is the
only national system to include commensals from healthy humans
but lacks data from companion animals. The Netherlands has ex-
tended its surveillance in foodborne microbes to include non-
animal origin foodstuffs.
The recommendations for a One Health approach at a global level
by JPIAMR, the White House and WHO will hopefully influence those
national systems committed to being part of the global system. The
significant challenge to build capacity at local and national levels
persists. Modern technology may hold some solutions to data man-
agement, but using high-tech systems in remote, underdeveloped
regions may be difficult. Yet developing countries will potentially
have the greatest influence on the future of AMR. Global invest-
ment is needed for capacity-building to improve the control of
hospital infections, to control antimicrobial usage in food-producing
Table 2
Summary of costs and benefits of One Health antimicrobial resistance (AMR) surveillance and resultant interventions.
Integrating AMR surveillance to a One Health level
Costs Benefits
1. Costs of design and setup, including time to agree on
common goals, new roles and duties, dispersal of
funding and resolving issues of conflict.
2. Costs of training staff in interdisciplinary work.
3. Costs of additional staff, expert consultants, joint
consultations and meetings.
4. Costs of collating additional data, and joint analysis
and communication of results.
5. Additional costs for extending the breadth and
depth of coverage of surveillance.
1. Improved service delivery.
2. Improved efficiency by sharing scarce resources or better use of underutilised resources.
3. Social capital gains through sharing skillsets and networking.
4. Improved synergies between empirical, social, environmental and ecological sciences.
5. Enriched and more efficient research outcomes.
6. More timely and accurate identification of risks through broader surveillance and integration.
7. Improved, more timely and efficient interventions based on improved risk assessments.
Integrated interventions arising from One Health surveillance
Costs Benefits
1. Increased costs of wider interventions across human
and animal health and the environmental sectors.
2. Potential increased costs of livestock production
through use of improved biosecurity in contrast to
prophylactic use of antibiotics.
1. Broader benefits across sectors arising from a systems approach versus narrow reactionary solutions.
2. Improved and broader valuation of benefits by including intangible societal and environmental
benefits.
3. Reduced healthcare costs (prevention of longer hospitalisation, more expensive drugs, intensive
infection control measures, etc.)
4. Decreased morbidity and mortality.
5. Prevention of reduced workforce productivity owing to prolonged recovery or caring for relatives.
6. Prevention of costs of litigation against hospital and staff.
7. Prevention of lost income through reduced cross-border travel and tourist income, and from
reduced trade in live animals and food of animal origin.
8. Reduced cost of animal health care and infection control in food-producing animal systems.
9. Prevention of increased cost in foodstuffs from animal origin.
10. Improved consumer confidence in food safety.
11. Improved ecosystem resilience.
426 K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
animals and to control the sale of antibiotics without prescription
and counterfeit drugs [39,40]. The inclusion of their surveillance data
is therefore crucial.
The WHO identified data quality as the major shortcoming of
existing systems. Without standardised laboratory techniques and
reconcilable data, meaningful analysis and constructive interven-
tions will fall short of expectations. Once laboratory standards and
methods of data recording are agreed on, the surveillance systems
should develop and extend to incorporate as much of the One Health
framework as possible, with increasing degrees of integration.
8. Conclusion
As the increase in AMR continues and fewer new drugs are being
developed, calls for action to avert the impending crisis of a ‘post-
antibiotic era’ are being heard. To promote effectiveness and
economic efficiency, interventions need to be designed from sound
evidence gained from surveillance. A broad One Health approach
to the evidence-gathering surveillance, data analysis, intervention
design and evaluation is proposed. Given the scale of the problem
and the expected socioeconomic costs, the additional monetary,
social and time investments are likely to be recovered by the re-
sulting benefits, which include quantifiable financial efficiencies and
improved human and animal health outcomes. In addition, if one
looks broadly and includes the less tangible benefits to society (open
trade and travel), animal welfare, ecosystem health and environ-
mental resilience, then the business case for a One Health approach
to AMR surveillance is strengthened.
Based on the framework presented in this paper, the develop-
ment of a One Health surveillance system is called for. Its foundation
must be based on standard laboratory techniques and data man-
agement, which can be integrated, compared and interpreted at all
levels. This will require global and local governance to work to-
gether. Widening the scope of surveillance to include all aspects
within the proposed framework can be built on this foundation over
time but may require a shift in institutional mindsets.
Funding: This work was funded by the Food and Agriculture Or-
ganization (FAO) of the United Nations [Project code 3058, grant
reference OSRO/INT/602/USA, ‘Support to present a business case
for One Health under the Human–Animal Interface’], the Royal Vet-
erinary College’s Internal Grant Scheme [Project Code 2958 ‘Metrics
for One Health benefits: key inputs to create an economic evi-
dence base’] and partial funding from the Leverhulme Centre for
Integrative Research on Agriculture and Health (LCIRAH) (Hat-
field, UK), grant reference F/10 208/A. The sponsors were not involved
in creating this document.
Competing interests: None declared.
Ethical approval: Not required.
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Queenan OHAMRS

  • 1. A One Health approach to antimicrobial resistance surveillance: is there a business case for it? Kevin Queenan a, *, Barbara Häsler a,b , Jonathan Rushton a a Veterinary Epidemiology, Economics and Public Health Group, Department of Production and Population Health, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK b Leverhulme Centre for Integrative Research on Agriculture and Health (LCIRAH), Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK A R T I C L E I N F O Article history: Received 19 February 2016 Accepted 18 June 2016 Keywords: Antimicrobial resistance AMR Surveillance One Health Business case Economics A B S T R A C T Antimicrobial resistance is a global problem of complex epidemiology, suited to a broad, integrated One Health approach. Resistant organisms exist in humans, animals, food and the environment, and the main driver of this resistance is antimicrobial usage. A One Health conceptual framework for surveillance is presented to include all of these aspects. Global and European (regional and national) surveillance systems are described, highlighting shortcomings compared with the framework. Policy decisions rely on eco- nomic and scientific evidence, so the business case for a fully integrated system is presented. The costs of integrated surveillance are offset by the costs of unchecked resistance and the benefits arising from interventions and outcomes. Current estimates focus on costs and benefits of human health outcomes. A One Health assessment includes wider societal costs of lost labour, changes in health-seeking behaviour, impacts on animal health and welfare, higher costs of animal-origin food production, and reduced con- sumer confidence in safety and international trade of such food. Benefits of surveillance may take years to realise and are dependent on effective and accepted interventions. Benefits, including the less tangi- ble, such as improved synergies and efficiencies in service delivery and more timely and accurate risk identification, should also be recognised. By including these less tangible benefits to society, animal welfare, ecosystem health and resilience, together with the savings and efficiencies through shared resources and social capital-building, a stronger business case for a One Health approach to surveillance can be made. © 2016 Elsevier B.V. and International Society of Chemotherapy. All rights reserved. 1. Introduction and background In 2001, the World Health Organization (WHO) described anti- microbial resistance (AMR)1 as a global problem requiring a global response [1], but until recently it has failed to gain the urgent at- tention it deserves. Economic evidence is used as a tool to prioritise policy decisions and it has been argued that previous estimates of the health cost of AMR have been too negligible [2] and they have failed to consider the wider impacts on health care [3]. However, recently more alarming estimates of AMR have appeared in the lit- erature. The European Commission claimed that costs attributed to resistant bacterial infections amounted to €1.5 billion annually [4]. Healthcare systems in the USA estimate the additional cost of antimicrobial-resistant infections to be US$20 billion a year and pro- ductivity losses to be US$35 billion a year [5]. The UK government- commissioned ‘Review of antimicrobial resistance’ estimated that drug- resistant infections could cause 10 million human deaths annually by 2050, with total costs by this date of US$100 trillion in lost output [6]. Disease surveillance provides evidence for informed decisions on interventions, and AMR surveillance is no exception [7,8]. Sur- veillance of AMR is critical for impact evaluation of, for example, interventions that change guidelines on antimicrobial usage or in- fection control [9]. Moreover, it provides information on AMR emergence and occurrence relevant for the public, patients, health- care providers, governmental agencies and researchers [7]. Despite the WHO calling for local, national and global AMR sur- veillance systems to be established [8], gaps in surveillance remain, primarily through lack of capacity and integration [10]. The US Na- tional Action Plan proposed the strengthening of a ‘One Health’ national surveillance system (for humans, animals and the envi- ronment) with improved international collaboration and capacity [11]. One Health, however, also refers to a broad, systems-based ap- proach to complex problems [12]. It is therefore suited to AMR surveillance because it considers the underlying structural factors * Corresponding author. Veterinary Epidemiology, Economics and Public Health Group, Department of Production and Population Health, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK. Fax: +44 0 1707 666333. E-mail address: kqueenan3@rvc.ac.uk (K. Queenan). 1 Although by definition AMR refers to resistance of all microbes including bac- teria, viruses, parasites and fungi, this paper and the majority of the literature use the term with a bias towards bacterial resistance. http://dx.doi.org/10.1016/j.ijantimicag.2016.06.014 0924-8579/© 2016 Elsevier B.V. and International Society of Chemotherapy. All rights reserved. International Journal of Antimicrobial Agents 48 (2016) 422–427 Contents lists available at ScienceDirect International Journal of Antimicrobial Agents journal homepage: www.elsevier.com/locate/ijantimicag
  • 2. that influence AMR, including the sociopolitical, material, biolog- ical and economic factors [13]. A One Health approach also includes an analysis of the context and institutional environment in which decisions are made across all levels of society [14]. In recognition of the above, this paper proposes a framework to promote a One Health surveillance system for AMR. Resistance is a global concern, with no regard for national borders, degree of healthcare sophistication or national gross domestic product (GDP) [15]. Despite this, not all regions of the world have promoted in- tegrated AMR surveillance systems. To assess the level of integration, strengths, challenges and weakness, literature on the current global, regional (European) and selected European national surveillance systems is reviewed and positioned against the proposed frame- work. Whilst the economic benefits for a One Health approach to zoonotic infectious disease surveillance have been published else- where [16–19], this paper builds a business case for a One Health approach to AMR surveillance. 2. Why a One Health approach and fully integrated surveillance system? The discussion of AMR is often focussed on human health out- comes. However, a broader consideration of the impacts on animal and environmental health is essential. Prescott discussed the complex epidemiology of AMR and stated that ‘resistance anywhere is re- sistance everywhere’ [20]. AMR is described as an ecological problem by Radhouani et al [21], and as ‘a highly multifaceted topic at the interface of human, animal and plant health, food hygiene and en- vironmental science’ by Butaye et al [22]. Antimicrobial usage (more specifically antibiotics)2 and the re- sultant selective pressure have been recognised as the main drivers for AMR [23,24]. It is therefore essential to link antimicrobial usage data with AMR surveillance data when considering methods for AMR containment. The combined surveillance would also facilitate moni- toring of the impact of interventions aimed to improve antibiotic stewardship and reduce consumption [9]. The widespread use of biocidal soaps and gels versus simple soap handwashing and the benefits of potentially reducing the spread of institutional infec- tions versus contributing to AMR are other areas for consideration [25]. Rushton stated that antimicrobials should be seen as a common good [14]. In light of this, human behaviour and attitudes around antibiotic prescribing and use should be considered both in human and veterinary medicine. Decisions around antimicrobial usage in livestock should consider the trade-offs that occur between restor- ing animal health and productivity, provision of animal welfare and impacts on livelihoods, hunger and poverty alleviation versus the risk of driving resistance [14]. Prescribing decisions of companion animal veterinarians are also influenced by affordability, ease of ad- ministration and perceived compliance [26]. The environmental impact of the management of human effluent, waste from live- stock and aquaculture facilities and from manufacturers of pharmaceuticals is recognised as a potential hotspot for AMR [27]. These aspects are yet more evidence that a broad, contextual or institutional analysis is required when considering the use or misuse of antimicrobials [14]. A systems-based approach to surveillance will better identify critical control points thereby improving effective- ness and economic efficiency. 3. One Health framework for antimicrobial resistance surveillance A conceptual framework for a One Health approach to AMR sur- veillance is proposed here and is illustrated in Fig. 1. It centralises and integrates surveillance both of antibiotic usage or consump- tion for humans and animals with AMR data from humans, animals, food and the environment. Consumption data in humans are gathered in hospital and com- munity settings, whilst in animals they are gathered at the species level, i.e. food-producing animals (including fish), companion animals and wildlife. AMR surveillance in humans includes invasive sam- pling of clinical cases from hospital and community care settings as well as non-invasive sampling of commensals. In food-producing animals, isolates are accessed from clinical cases and commensals from healthy animals (available at slaughter). Similarly, samples of clinical cases in companion animals and wildlife are easily ac- cessed through veterinarians, although commensals from both groups, especially wildlife, may be less feasible. Surveillance of AMR in organisms isolated from food includes food originating from 2 In the context of usage, the literature’s focus has been on antibiotics and the impact on resistance in bacteria. Fig. 1. An interconnected and integrated One Health surveillance framework that puts at its centre antimicrobial resistance and antimicrobial consumption. 423K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
  • 3. animals and plants (zoonotic pathogen surveillance from the former and commensals from both). Environmental surveillance includes samples from water sources and soil. Data collected within the various categories require an inte- grated analysis, facilitated by teams with experience across the sectors. Similarly, interpretation of the analysis requires teams of sectoral experts who also possess intersectoral knowledge and un- derstanding and the collaborative skills to work with those from other sectors, including social scientists and behaviour change experts. This is to ensure a One Health approach to developing the subsequent recommendations. A centralised programme is required to set standards for data collection, which is critical at all levels for ease of analysis and in- terpretation. This will also improve communication and networking between disciplines and sectors through shared meetings, discus- sions and report editing. Centralised leadership and budgeting will be responsible for sup- porting and enabling peripheral capacity and compliance. However, this ideal, multidimensional, integrated surveillance may be diffi- cult to achieve across all categories given the high level of capacity and logistics required and the commonly found barriers between siloed institutions. A tiered approach to integration may assist in building capacity. Within each tier, globally recognised tech- niques and standards must be adopted and adhered to. The initial tier would involve relatively standard collection, sharing and anal- ysis of data and therefore involve less integrated interpretation. The progression into the higher tiers would involve broadening data col- lection sources (from Fig. 1). This would require a shift in institutional mindsets to support the increasing degrees of co-operation and in- tegration required to facilitate the analysis and interpretation of results and evolution of joint recommendations. 4. A review of current surveillance systems, from global to local A review of the current global and European (regional and na- tional) surveillance systems was conducted to identify degrees of integration, with attention to AMR and usage data, sectoral inte- gration, and which species and which food types and environmental elements were included in sampling. 4.1. Global systems The 2008 WHO Advisory Group on Integrated Surveillance of An- timicrobial Resistance (AGISAR) has 31 internationally renowned expert advisors including representatives from the World Organisation for Animal Health (OIE) and the Food and Agricul- ture Organization (FAO). Their aims include developing standardised sampling techniques and methodology, providing expert advice, pro- moting information sharing and supporting capacity-building for AMR surveillance and antimicrobial usage in member states. The Global Foodborne Infections Network (GFN) has public health, veterinary and food-sector professionals, all working towards a global integrated AMR surveillance system. CODEX Alimentarius (commissioned by the WHO and FAO) in- cludes a task force to integrate AMR surveillance in humans with that in food-producing animals, crops and food. WHONET is a WHO initiative to support harmonisation of global surveillance data by providing free software and training to labo- ratories in over 100 countries within all six WHO regions. The software facilitates standardised data collection and analysis and also informal sharing and networking. The Transatlantic Taskforce on Antimicrobial Resistance (TATFAR) was established in 2009 as a collaboration between the USA and the European Union (EU). It aims to promote appropriate use of antimicrobials in human and veterinary medicine, to prevent re- sistant infections in hospital and communities and to improve development of new antimicrobials. The Joint Programming Initiative on Antimicrobial Resistance (JPIAMR) is a research group that co-ordinates global research in AMR. Their One Health research agenda includes AMR in humans, animals and the environment. 4.2. Regional (European) systems The European Centre for Disease Prevention and Control (ECDC) conducts surveillance for AMR and antibiotic consumption in human health through several networks. • The European Antimicrobial Resistance Surveillance Network (EARS-Net) provides guidance to members on data collection, management, analysis and validation. It collates data from over 900 public health laboratories, which process samples from clin- ical cases in over 1400 hospitals in 30 EU/European Economic Area (EEA) countries. • The European Surveillance of Antimicrobial Consumption Network (ESAC-Net) collates data on systemic use of antibiot- ics, antifungals and antivirals in hospital and community sectors from 32 EU/EEA countries. • The European Food and Waterborne Diseases and Zoonoses Network (FWD-Net) is responsible for surveillance of human pathogens from water, food or animal contact. The data con- tribute to the European Food Safety Agency (EFSA) and ECDC annual summary report. • The Healthcare Associated Infection Network (HAI-Net) co- ordinates AMR surveillance and antimicrobial use in acute (intensive care) and long-term care facilities and the surveil- lance of surgical site infections. Surveillance of AMR in food-producing animals and food prod- ucts, as well as veterinary antibiotic consumption, is covered by the following: • The European Centre for the Study of Animal Health (CEESA) col- lects standardised AMR data for a central laboratory, from healthy animals at slaughter and clinically ill food-producing and com- panion animals. • The European Surveillance of Veterinary Antimicrobial Con- sumption (ESVAC) aims to collect harmonised data on the sales of veterinary antimicrobials (from wholesalers, veterinarians and pharmacies) to enable comparison with human consumption data. Its fourth annual report [28] included data from ca. 95% of food-producing animals in 26 EU/EEA countries. • The EFSA collates AMR data within its surveillance of zoonoses and disease outbreaks from food and food-producing animals. It supports EU members, providing guidelines on standardising sampling and processing, so as to harmonise data for analysis. It produces an annual summary report in conjunction with the ECDC. In addition, the ECDC facilitates collaboration of surveillance groups with the European Committee on Antimicrobial Suscepti- bility Testing (EUCAST) and the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). ESCMID has been active for over 25 years, with a wide range of study groups, some concerned with specific disease agents and others covering anti- microbial policy (ESGAP), AMR surveillance (ESGARS) and veterinary microbiology (ESGVM). In 2012, building on the success of the ECDC programmes, EARS- Net was expanded and the Central Asia and European Surveillance of Antimicrobial Resistance (CAESAR) network was established. 424 K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
  • 4. 4.3. National systems The WHO’s global report on surveillance of AMR [10] is based on data from the 129 contributing member states. The report high- lighted individual national systems that attempt to integrate surveillance in humans, food-producing animals and food (Table 1). Several national systems within EU states have been guided towards integration through the direction of the European region- al systems as mentioned in the previous section. Longstanding examples include the following: (i) The Danish Integrated Antimicrobial Resistance Monitoring and Research Program (DANMAP) was established in 1995 as a collaborative programme between the Ministry of Health and the Ministry of Food, Agriculture and Fisheries. DANMAP has implemented a ‘farm to fork to sickbed’ approach to sur- veillance [29] to include the whole supply chain. Sampling includes human and animal clinical cases, healthy animals (randomly at slaughter) and locally produced and imported meat products at wholesale and retail outlets. Consumption data are collected from hospitals, primary healthcare centres and pharmacies. Veterinary medicine usage is registered at a species level [food-producing animals (including fish) and companion animals] by veterinarians, pharmacies and feed mills. (ii) The Swedish Strategic Programme Against Antibiotic Resis- tance (STRAMA), founded in 1995, aims to preserve antimicrobial agent effectiveness in public health. The Swedish Veterinary Antimicrobial Resistance Monitoring Programme (SVARM) was established in 2000. STRAMA has produced an annual report (SWEDRES) on antibiotic use and resistance in humans since 2001, whilst SVARM’s annual report covered AMR surveillance in zoonotic bacteria, specific animal patho- gens, commensal enteric bacteria and bacteria from food of animal origin. Since 2011, a combined, integrated SWEDRES/ SVARM annual report has been published, demonstrating intersectoral collaboration. (iii) The Netherlands has, since 2003, produced NethMap, an annual report on AMR and antibiotic consumption trends in humans. MARAN, the veterinary surveillance system, has done the same for food-producing animals and also includes isolates from vegetables, fruits and herbs. Since 2012, a single, combined (NethMap-MARAN) report has been published. 5. Challenges and shortcomings, recent developments and future improvements The review demonstrates evidence of broader sampling, inte- gration and shared analysis, however thus far no fully integrated and standardised surveillance system for AMR and antimicrobial usage, which functions both locally and globally, exists. A lack of data quantity and quality persists, the latter affected by a lack of standardisation [30]. There is still insufficient comparable data of AMR in humans and livestock to develop global mapping of re- sistance and to allow accurate comparisons between humans, various livestock species, industries, countries and regions [31]. In 2012, the WHO published results of a survey of existing sur- veillance networks [32]; 5 international and 22 national networks responded. Only 30% had a nationally co-ordinated body, whilst <40% had formal quality assurance requirements and antimicrobial usage data were generally absent. In the WHO’s global report on surveil- lance of AMR [10], there was no formal consensus on methodology and data collection amongst the 129 contributing member states. At the European level, although EARS-Net advises and encourages standardisation using EUCAST guidelines, only 64% of the partici- pating laboratories do so [23]. Global systems are reliant on data collected nationally. Therefore, standards within data collection need to be applied at source to allow meaningful interpretation at all levels, which will require significant investment in developing ca- pacity. Therefore, in the next section we discuss a business case for a One Health approach to AMR surveillance. 6. The business case for a One Health approach to antimicrobial resistance surveillance Whilst Babo Martins et al provided a framework for a broad eco- nomic assessment of integrated zoonotic disease surveillance in a One Health context [19], publications showing direct measureable impacts of AMR surveillance and interventions from a One Health perspective were not found. Similarities exist between the busi- ness case for AMR surveillance and of emerging zoonotic infectious diseases. In both cases their unpredictable nature makes econom- ic evaluation dependent on assumptions and/or predictive modelling, which are often subject to considerable uncertainty. Appreciating the broad complexity and interconnectivity of human, animal and environmental outcomes, a One Health, systems-thinking ap- proach is needed to measure the benefits of investment in integrated surveillance. Evaluation of economic and empirical scientific aspects must be blended with an appreciation of the social, cultural and Table 1 Antimicrobial resistance surveillance systems [10]. Surveillance system, country Surveillance of resistant bacteria from: Bacterial species included Healthy animals Diseased animals Food Healthy humans Diseased humans Salmonella Campylobacter Escherichia coli Enterococci Animal pathogens CIPARS, Canada X X X X X X X X DANMAP, Denmark X X X X X X X X X X FINRES-Vet, Finland X X X X X X X X X GermVet, Germany X X X X X ITAVARM, Italy X X X X X X X X JVARM, Japan X X X X X NARMS, USA X X X X X X X X NethMap/MARAN, The Netherlands X X X X X X X X NORM/NORM-VET, Norway X X X X X X X X X ONERBA, France X X X X X X X X X SWEDRES/SVARM, Sweden X X X X X X X X X CIPARS, Canadian Integrated Program for Antimicrobial Resistance Surveillance; DANMAP, Danish Integrated Antimicrobial Resistance Monitoring and Research Program; FINRES-Vet, Finnish Veterinary Antimicrobial Resistance Monitoring and Consumption of Antimicrobial Agents; GermVet, German National Antibiotic Resistance Monitor- ing; ITAVARM, Italian Veterinary Antimicrobial. Resistance Monitoring; JVARM, Japanese Veterinary Antimicrobial Resistance Monitoring System; NARMS, National Antimicrobial Resistance Monitoring System; MARAN, Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in The Netherlands; ONERBA, Observatoire National de l’Épidémiologie de la Résistance Bactérienne aux Antibiotiques; SVARM, Swedish Veterinary Antimicrobial Resistance Monitoring Programme. 425K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
  • 5. ecological aspects [33]; the less tangible and non-monetary out- comes should be considered in addition to the monetary. These less tangible benefits include knowledge creation, social and intellec- tual capital, reduced anxiety, political reassurance and technical capacity-building. Whilst these are not always easily quantifiable, they should be considered none the less [19]. Table 2 summarises the costs and benefits envisaged from in- tegrating surveillance of AMR to a One Health level and also the costs and benefits of the integrated interventions arising from the One Health surveillance. Although costs are incurred in the setup of or conversion into a One Health system, savings are expected from the effects of shared and more efficient use of resources, shared running costs and im- proved outcomes. Using the H5N1 (highly pathogenic avian influenza) campaign as an example, the World Bank estimated cost savings of 10–30% from joint investment and 20–40% in costs of ongoing surveillance through shared staff and facilities. Further savings in training and research are estimated at 5–10% [34]. Surveillance benefits primarily relate to those arising from the interventions it spawns. Interventions are often delayed whilst suf- ficient data are collected and analysed. Benefits may not be immediate (e.g. the impact on public health outcomes from reduced antimi- crobial use) and may also be confounded by several factors over time [35]. Global travel is an example; despite Denmark’s attempts to control resistance in Campylobacter, 37% of campylobacteriosis cases in humans were related to international travel, with a higher pro- portion of these being resistant compared with domestic cases [29]. Positive knock-on effects also need to be recognised. Den- mark’s integration of antimicrobial consumption data with resistance data identified specific links, resulting in improved public aware- ness and government policy [36], which included a ban on the use of certain antibiotics in livestock and restrictions on veterinarians’ profits from antibiotic sales [37]. In addition, a voluntary ban against using cephalosporins and fluoroquinolones in food-producing animals followed. As a result, food-producing animals in Denmark consume 80% less antimicrobials per kg of meat produced than those in the USA [37]. A greater understanding is required of the wider implications and costs of AMR on society. Implications include changes in health- seeking behaviour, e.g. avoiding invasive procedures because of the (perceived) risk of untreatable infections [2], increased hospital in- fection control measures, litigation, and reduced international travel and trade [38]. Furthermore, reports on the costs of unchecked AMR fail to consider the impact on the food-producing animal sector and the effect on livestock-dependent communities and national econo- mies. The costs of untreatable livestock diseases, increased biosecurity costs and the costs of lost consumer confidence in the safety of food of animal origin as well as animal welfare issues need to be included. 7. Discussion Recent calls to improve the integration of AMR and consump- tion surveillance are welcomed. This complex, interconnected problem with negative externalities will require international intersectoral collaboration. It therefore favours the application of a One Health approach to the surveillance systems, the interven- tions and the evaluation of outcomes. The European national surveillance systems reviewed in this paper all fall short of the One Health framework presented above, with none mentioning the environment or wildlife. DANMAP is the only national system to include commensals from healthy humans but lacks data from companion animals. The Netherlands has ex- tended its surveillance in foodborne microbes to include non- animal origin foodstuffs. The recommendations for a One Health approach at a global level by JPIAMR, the White House and WHO will hopefully influence those national systems committed to being part of the global system. The significant challenge to build capacity at local and national levels persists. Modern technology may hold some solutions to data man- agement, but using high-tech systems in remote, underdeveloped regions may be difficult. Yet developing countries will potentially have the greatest influence on the future of AMR. Global invest- ment is needed for capacity-building to improve the control of hospital infections, to control antimicrobial usage in food-producing Table 2 Summary of costs and benefits of One Health antimicrobial resistance (AMR) surveillance and resultant interventions. Integrating AMR surveillance to a One Health level Costs Benefits 1. Costs of design and setup, including time to agree on common goals, new roles and duties, dispersal of funding and resolving issues of conflict. 2. Costs of training staff in interdisciplinary work. 3. Costs of additional staff, expert consultants, joint consultations and meetings. 4. Costs of collating additional data, and joint analysis and communication of results. 5. Additional costs for extending the breadth and depth of coverage of surveillance. 1. Improved service delivery. 2. Improved efficiency by sharing scarce resources or better use of underutilised resources. 3. Social capital gains through sharing skillsets and networking. 4. Improved synergies between empirical, social, environmental and ecological sciences. 5. Enriched and more efficient research outcomes. 6. More timely and accurate identification of risks through broader surveillance and integration. 7. Improved, more timely and efficient interventions based on improved risk assessments. Integrated interventions arising from One Health surveillance Costs Benefits 1. Increased costs of wider interventions across human and animal health and the environmental sectors. 2. Potential increased costs of livestock production through use of improved biosecurity in contrast to prophylactic use of antibiotics. 1. Broader benefits across sectors arising from a systems approach versus narrow reactionary solutions. 2. Improved and broader valuation of benefits by including intangible societal and environmental benefits. 3. Reduced healthcare costs (prevention of longer hospitalisation, more expensive drugs, intensive infection control measures, etc.) 4. Decreased morbidity and mortality. 5. Prevention of reduced workforce productivity owing to prolonged recovery or caring for relatives. 6. Prevention of costs of litigation against hospital and staff. 7. Prevention of lost income through reduced cross-border travel and tourist income, and from reduced trade in live animals and food of animal origin. 8. Reduced cost of animal health care and infection control in food-producing animal systems. 9. Prevention of increased cost in foodstuffs from animal origin. 10. Improved consumer confidence in food safety. 11. Improved ecosystem resilience. 426 K. Queenan et al. / International Journal of Antimicrobial Agents 48 (2016) 422–427
  • 6. animals and to control the sale of antibiotics without prescription and counterfeit drugs [39,40]. The inclusion of their surveillance data is therefore crucial. The WHO identified data quality as the major shortcoming of existing systems. Without standardised laboratory techniques and reconcilable data, meaningful analysis and constructive interven- tions will fall short of expectations. Once laboratory standards and methods of data recording are agreed on, the surveillance systems should develop and extend to incorporate as much of the One Health framework as possible, with increasing degrees of integration. 8. Conclusion As the increase in AMR continues and fewer new drugs are being developed, calls for action to avert the impending crisis of a ‘post- antibiotic era’ are being heard. To promote effectiveness and economic efficiency, interventions need to be designed from sound evidence gained from surveillance. A broad One Health approach to the evidence-gathering surveillance, data analysis, intervention design and evaluation is proposed. Given the scale of the problem and the expected socioeconomic costs, the additional monetary, social and time investments are likely to be recovered by the re- sulting benefits, which include quantifiable financial efficiencies and improved human and animal health outcomes. In addition, if one looks broadly and includes the less tangible benefits to society (open trade and travel), animal welfare, ecosystem health and environ- mental resilience, then the business case for a One Health approach to AMR surveillance is strengthened. Based on the framework presented in this paper, the develop- ment of a One Health surveillance system is called for. Its foundation must be based on standard laboratory techniques and data man- agement, which can be integrated, compared and interpreted at all levels. This will require global and local governance to work to- gether. Widening the scope of surveillance to include all aspects within the proposed framework can be built on this foundation over time but may require a shift in institutional mindsets. Funding: This work was funded by the Food and Agriculture Or- ganization (FAO) of the United Nations [Project code 3058, grant reference OSRO/INT/602/USA, ‘Support to present a business case for One Health under the Human–Animal Interface’], the Royal Vet- erinary College’s Internal Grant Scheme [Project Code 2958 ‘Metrics for One Health benefits: key inputs to create an economic evi- dence base’] and partial funding from the Leverhulme Centre for Integrative Research on Agriculture and Health (LCIRAH) (Hat- field, UK), grant reference F/10 208/A. The sponsors were not involved in creating this document. Competing interests: None declared. Ethical approval: Not required. References [1] World Health Organization. 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