The current issue and full text archive of this journal is available on Emerald Insight at:

www.emeraldinsight.com/2059-4631.htm

IJHG
21,3
Antimicrobial stewardship
through a one health lens
Observations from Washington State
114 Marisa Anne D’Angeli, Joe B. Baker, Douglas R. Call,
Received 21 February 2016 Margaret A. Davis, Kelly J. Kauber, Uma Malhotra,
Revised 13 June 2016
Accepted 13 June 2016
Gregory T. Matsuura, Dale A. Moore, Chris Porter, Paul Pottinger,
Virginia Stockwell, Carol Wagner, Ron Wohrle, Jonathan Yoder,
Leah Hampson Yoke and Peter Rabinowitz
(Information about the authors can be found at the end of this article.)

Abstract
Purpose – Antibiotic resistance (AR) is a global health crisis that is attracting focussed attention from
healthcare, public health, governmental agencies, the public, and food producers. The purpose of this
paper is to describe the work in Washington State to combat resistance and promote antimicrobial
stewardship from a one health perspective.
Design/methodology/approach – In 2014, the Washington State Department of Health convened a
One Health Steering Committee and two workgroups to focus on AR, the One Health Antimicrobial
Stewardship work group and the One Health Antimicrobial Resistance Surveillance work group. The
group organized educational sessions to establish a basic understanding of epidemiological factors
that contribute to resistance, including antibiotic use, transmission of resistant bacteria, and
environmental contamination with resistant bacteria and antibiotic residues.
Findings – The authors describe the varied uses of antibiotics; efforts to promote stewardship in
human, and animal health, including examples from the USA and Europe; economic factors
that promote use of antibiotics in animal agriculture; and efforts, products and next steps of
the workgroups.
Originality/value – In Washington, human, animal and environmental health experts are working
collaboratively to address resistance from a one health perspective. The authors are establishing a
multi-species resistance database that will allow tracking resistance trends in the region. Gaps include
measurement of antibiotic use in humans and animals; integrated resistance surveillance information;
and funding for AR and animal health research.
Keywords One health, Antibiotic resistance, Antibiotic stewardship, Washington State
Paper type Viewpoint

Antibiotic resistance (AR) is a global health crisis (World Health Organization, 2012)
that threatens patient care, public health, agriculture, economic growth, and
national security (King, 2014). It has recently attracted increasing attention from
healthcare professionals, public health officials, federal governments, international
agencies, the public, and food producers. Despite seven decades of warnings, AR
continues to increase (Centers for Disease Control and Prevention, 2013). It is clear
that AR is a threat to all – healthy and vulnerable humans in high- and low-income
nations, pets and animals raised for food – and that cooperative, collaborative
International Journal of Health
Governance global action is essential to mitigate this threat. The purpose of this paper is to
Vol. 21 No. 3, 2016
pp. 114-130
describe Washington’s statewide effort to combat antibiotic resistant bacteria from a
© Emerald Group Publishing Limited one health perspective, and to present our findings and observations about the
2059-4631
DOI 10.1108/IJHG-02-2016-0009 challenges we face.
 In 2014, the Washington State Department of Health established a statewide One Antimicrobial
Health Steering Committee with representation from State Departments of Agriculture, stewardship
Fish and Wildlife, and Health; academic researchers from University of Washington
Center for One Health Research and Washington State University Paul G. Allen School
for Global Animal Health; human and animal health experts; the Washington State
Veterinary Medical Association; and the Governor’s office. The committee’s goal is to
improve knowledge, communication, cooperation, and coordination in responding to 115
health issues that cross the human and animal health sectors. Many zoonoses and
emerging infections are worthy of attention using a one health lens. However, in
response to President Obama’s National Strategy for Combating AR that calls for a one
health approach, the Washington One Health committee chose to focus first on AR.
The complex epidemiology of AR guides our work in Washington. Figure 1
illustrates the principal transfer pathways for antibiotics and AR genes between
humans, animals, food, and the environment. We believe a one health approach to
combating AR should be based on a comprehensive understanding of how, where and
why antibiotics are used, how previously susceptible bacteria acquire new resistance
traits, and what factors favor amplification and transmission of resistant bacteria.
The main factors promoting resistance have been well documented in the literature and
will receive only a cursory review here.
Antibiotic use – Most antibiotics are derived from naturally produced compounds
that can be found in association with existing AR traits (Cox and Wright, 2013), but
the prevalence of acquired resistance has dramatically increased due to selection
pressure imposed through large-scale use in human medicine. Clinically important
AR is often identified within a relatively short time after introduction of new
antibiotics (Levy et al., 1976). In some cases, withdrawal of antibiotics results in
reduced AR (Dutil et al., 2010), but not always (Enne, 2010). Resistance mechanisms
include mutations, such as spontaneous point mutations (Hooper and Jacoby, 2015),
or acquisition of entire functional genes coding for resistance traits via conjugation,
transduction, or transformation processes (Huddleston, 2014). Occurrence of

Antibiotic use

Crops

Food

Humans

Animals
Environment Figure 1.
(soil and water) Principal transfer
pathways for
antibiotics and
antibiotic resistance
genes between
humans, animals,
food, and the
Antibiotics environment
Antibiotic resistance genes
IJHG mutations and horizontal gene transfer events are considered stochastic processes,
21,3 but evidence suggests that exposure to some antibiotics may increase mutation and
horizontal gene transfer rates via the SOS response (an inducible DNA repair system),
phage induction, and by influencing gene expression (Andersson and Hughes, 2014;
Blazquez et al., 2001).
Transmission of antibiotic resistant bacteria – the primary transmission routes for
116 resistant bacteria are between people in healthcare settings (Magill et al., 2014) and in
the community (Rafee et al., 2012); between people and animals, such as to and from
household pets (van Duijkeren et al., 2004; Harrison et al., 2014) and farm animals
(Fey et al., 2000; Harrison et al., 2013; Price et al., 2012); between livestock (Le Devendec
et al., 2011); between environmental systems such as soil and water; and between the
environment and living creatures (Blanco et al., 2009; Vieira et al., 2011), either directly,
or indirectly through food. The most significant routes of transmission likely vary by
setting, for example, in low resource settings with poor sanitation, contaminated water
could be a more significant route than in high-income countries.
De novo resistance generated in ecosystems – bacteria in water, soil, and sewage
may be acted upon by antibiotic residues and metabolites that result from industry,
runoff from agricultural uses, improper disposal of antibiotics, excreta from humans
and animals, and household uses. Improperly treated wastewater containing antibiotics
from pharmaceutical manufacturing has been documented in India (Fick et al., 2009).
The risk from antibiotic contamination generating resistance depends on the
environmental conditions, and concentration and bioavailability of antibiotics
(Youngquist et al., 2014, Subbiah et al., 2011).
Horizontal gene transfer – horizontal gene transfer between bacteria may result in
increased prevalence of a new resistance characteristic, particularly in the context of
antimicrobial selection pressure. This process of genetic mixing may occur between
different species of bacteria, such as between Klebsiella, E. coli, and Enterobacter. These
genera in the family Enterobacteriaceae are normally found in the stool of mammals and
birds and are common causes of healthcare- and community-associated infections. Plasmid-
mediated gene transfer is thought to be responsible for the rapid and alarming spread of
carbapenemase-producing Enterobacteriaceae around the world (Nordmann et al., 2011).
There is also concern that resistance genes from food sources may be transferred intra-
intestinally via whole bacterium transmission or mobile genetic elements and ultimately
cause extra-intestinal disease (Lazarus et al., 2015; Manges, 2016; Singer, 2015).
Our goal is to identify the most important causes of AR and interventions that are
low cost and high impact in order to maximize the effectiveness of our limited
resources. Toward this goal, Washington State’s Combating Antibiotic Resistant
Bacteria initiative identified the following 5 strategies for addressing AR: detect;
protect; prevent; innovate; and collaborate.
(1) detect includes surveillance and laboratory capacity to identify important
mechanisms of resistance;
(2) protect refers to reporting, notification, and communication about
epidemiologically important organisms, and promoting best practices in
infection control and biosecurity;
(3) prevent encompasses antibiotic stewardship, immunization, health
enhancement, and other novel interventions to prevent infections from
occurring;
 (4) innovate denotes development of new, better diagnostics and therapeutics, and Antimicrobial
improvements in health management; and stewardship
(5) collaborate represents local, regional, national, international and cross-
disciplinary work to comprehensively address resistance.

One-Health antimicrobial stewardship workgroup 117

The One Health Antimicrobial Stewardship workgroup convened in early 2015 and meets
quarterly. In addition to those represented on the steering committee, the workgroup
includes representatives of local health departments; Washington State University College
of Veterinary Medicine and Cooperative Extension; Centers for Medicare and Medicaid-
designated quality improvement organization for Washington; Washington State Hospital
Association, academic and practicing physicians and veterinarians; physician assistants;
nurse practitioners; pharmacists; microbiologists; horticultural experts; and economists.

Working together
Human and veterinary health care communities do not routinely work together on AR
and sometimes view each other with suspicion. An early one health goal was for our
human and animal health representatives to become more familiar with each other’s
“culture.” Members developed a vision and mission statement to define the group’s
purpose and goals in the first list below and, subsequently, defined common principles
for collaboration and communication which include showing mutual respect, seeking
win-win solutions, avoiding blame, and focussing on science (second list below).
Vision and Mission of the Washington One Health Antimicrobial Stewardship
Workgroup:
(1) Vision:
• Judicious use of antimicrobials in all species to maximize health, minimize
harm, and preserve effectiveness.
(2) Mission:
• represent key partners and stakeholders in human, animal, and plant
health;
• work collaboratively to promote judicious use of antimicrobials across all
sectors;
• identify gaps, strategize solutions, and mobilize resources to advance
antimicrobial stewardship;
• promote education and shared learning; and
• evaluate outcomes with a one health perspective.
Washington One Health Principles of Collaboration and Communication
The members of the Washington State One Health Steering Committee and its
subcommittees and workgroups acknowledge that the process of working across the
sectors of human health, animal health, and environmental health requires unique
processes of collaboration and communication. The principles underlying these
processes include the following:
• mutual respect for the perspectives and needs of the different disciplines;
IJHG • agreeing to work on solutions to complex problems that are “win-win” in terms of
21,3 simultaneously maximizing human, animal, and environmental health;
• agreeing that we will work whenever possible in a collaborative manner to develop
standards for best professional practices across sectors and not single out
particular sectors for “blame” or attribution regarding particular health issues;
• agreeing that we will focus on evidence based, scientific approaches for best
118
practices and conclusions regarding root causes of problems; and
• agreeing that when sharing data between sectors, integrated data will be
analyzed in a responsible manner based on science and not politics.
Members therefore agree to follow these principles in their professional involvement
and activities with the Steering Committee and workgroups.
The group’s early accomplishments served to publicize our collaborative effort and
recruit others to work in a similar manner to improve antibiotic use in all sectors.
Members authored a position statement for the Council of State and Territorial
Epidemiologists promoting antimicrobial stewardship in veterinary medicine and
animal agriculture (Council of State and Territorial Epidemiologists, 2015). We also
co-wrote and disseminated a “call to action” to improve antibiotic stewardship in
human and animal healthcare and in food animal production, citing specific actions for
consumers, prescribers, and food animal producers to improve antibiotic use. This
letter was signed by 18 state agencies and organizations in Washington, a novel
example of human and animal sectors working in common cause to combat AR
(Washington State Department of Health, 2015).

Increasing basic knowledge

To provide a basic working knowledge for workgroup members with different areas of
expertise, we coordinated a series of speakers on antibiotic use in human health care,
companion animal care, animal agriculture, fisheries, horticulture, and apiculture. We
learned that antibiotic use in human and companion animal medicine is surprisingly
similar, primarily for disease treatment and, less frequently, for infection prevention.
Most antibiotic applications in human and veterinary medicine in the USA require a
prescription. In high-income countries, companion animals may receive specialized
medical care similar to human medicine, such as chemotherapy and complex surgeries,
with a similar need for antibiotics to ensure success and prevent complications. In both
human and companion animal care, pharmaceutical advertising and detailing may
contribute to higher healthcare costs and inappropriate prescriptions through
promotion of newer, more expensive, broad-spectrum antibiotic agents. In human
healthcare, there is concern that certain elements of pharmaceutical promotion, such as
gifts, free meals, and speakers’ fees, may result in a conflict of interest for prescribers
(Ornstein et al., 2011). Unique to companion animal care, veterinarians often prescribe
and dispense medications generating almost 30 percent of their income from pharmacy
services (Arp, 2012) which may incentivize over-prescription.
Antibiotic use in food animals may be divided into three categories: therapeutic; sub-
therapeutic (preventive); and non-therapeutic (growth promotion). Non-therapeutic, or
growth-promoting antibiotics, are administered in low concentrations and generally
during early life. However, new Federal Drug Administration (FDA) rules require that
after December 2016, no antibiotics be used for growth promotion, and any in-feed or
water use of any antimicrobial for treatment will require a veterinary feed directive
(VFD), changes that should substantially reduce growth promotion uses (Food and Antimicrobial
Drug Administration (FDA), 2013). Therapeutic uses in food animals, as in humans and stewardship
companion animals, encompass treatment of infectious and control of infectious
disease. Prescriptions may be for a single animal (treatment) or for an entire group
when one or several are ill (control). Preventive antibiotics are administered in low
doses when animals are known to be vulnerable to infectious diseases, for example, in
times of physiologic stress such as during transportation, exposure to environmental 119
contamination, crowding, and weaning.
Other agricultural applications of antibiotics include aquaculture, although
compared to other countries, the USA is a relatively small producer (Food and
Agriculture Organization of the United Nations, 2015). The few antibiotics registered
for use in USA aquaculture are typically administered via feed and therefore will also
fall under the new FDA rules; thus oversight of antibiotics used in aquaculture will
increase as of January 2017. It is important to note that antibiotic use in food animals
requires a mandated wash-out period (withholding period) to allow complete
metabolism and excretion of antibiotics. As a consequence, even if food animals are
treated with antibiotics, adherence to defined withdrawal periods ensures the absence
of antibiotic residues in the food supply. These practices, unfortunately, are not
consistently applied in developing countries (Dipeolu and Alonge, 2002).
Other less commonly known uses of antibiotics occur in horticulture and apiculture.
Overall, plant uses of antibiotics account for only 0.1 percent of the total agricultural
use of antibiotics in the USA (McManus, 2014). Three antibiotics are registered for use
on tree fruits in the USA (pear, apple, peach, and nectarine), and less than half the
acreage is treated with antibiotics within a single year (Stockwell and Duffy, 2012).
Generally, antibiotics are not registered for field applications on annual crops
(e.g. grains or vegetables), conifers, or small fruits and berries. Similar to the
“withholding period” described for animal and aquaculture systems, there is a
mandated “pre-harvest interval” ensuring that antibiotics are not applied to fruit trees
at least a month before harvest. Consequently, antibiotic residues on harvested fruit are
not detected or, in rare cases, are detected at levels well below the tolerances set by
government agencies (Stockwell and Duffy, 2012). Numerous studies have not detected
a significant impact of antibiotic use on plants on the prevalence of AR genes in
bacteria residing on plants or in soils (McManus, 2014). Antibiotics are also fed to
honey bees to treat and prevent foulbrood disease. It is recommended that the
treatment be given in the early spring or late fall before the main honey flow begins to
avoid contamination of production honey. Antibiotic contamination of honey has been
documented, particularly Chinese honey, which was banned from importation by the
European Union (EU) (European Commission, 2013a).
Future educational topics for our group will include information about quantity and
sources of antibiotic residues in water and soil, environmental contamination with
antibiotic resistant bacteria from food animal operations, human solid waste, and
wastewater treatment facilities. The current practices regarding treatment of these
sources of bacterial contamination (e.g. composting) and the economics of stewardship,
particularly in food animal production will be additional foci for education.

Cross-pollination between sectors

The workgroup catalogued currently known stewardship activities in Washington.
This effort provided an opportunity to learn from counterparts and identify efforts that
might be adapted for use in another sector. A product of this cross-pollination was an
IJHG educational brochure for veterinarians on AR and stewardship (Washington State
21,3 Veterinary Medical Association, 2015). A second activity was a survey of Washington
State veterinarian practitioners on knowledge and practices regarding resistance and
stewardship. The survey results will guide future training and education for
veterinarians in Washington and has been submitted for publication (Heather Fowler,
personal communication, April 29, 2016). This accounting of activities also allowed a
120 comparison of the organizational structure and resources for antibiotic stewardship in
different sectors.

Antibiotic stewardship in human healthcare

Antimicrobial stewardship is a coordinated effort to promote appropriate use of
antibiotics resulting in improved patient outcomes and reduced bacterial resistance.
Antibiotic stewardship was originally described as the “4 Ds” – the right drug, dose,
duration, and de-escalation ( Joseph and Rodvold, 2008). In human healthcare,
implementing stewardship may be more straightforward than in food animal
production because antibiotics are primarily used therapeutically, and fewer economic
pressures encourage antibiotic use. Multiple sources suggest that antibiotics in human
healthcare are overprescribed (Fleming-Dutra et al., 2016; Hecker et al., 2003) and that
judicious antibiotic use can improve patient outcomes, reduce resistance and
Clostridium difficile infections, and lower healthcare costs (Davey et al., 2006; Fridkin
et al., 2014). Factors that promote over- and inappropriate antibiotic use include the
sometimes mistaken perception that patient satisfaction depends on receiving an
antibiotic; weighing the potential for a dangerous infection more heavily than potential
harms from antibiotic use; and inadequate knowledge of prescription guidelines.
A stewardship program devoted to supporting best practices has been shown to be
vital for sustained improvements in prescribing practices (Barlam et al., 2016). The core
elements of antimicrobial stewardship, which include leadership commitment,
accountability, expertise, action, tracking, reporting, and education, provide a
framework for implementing and evaluating an antibiotic stewardship program that
is adaptable to different care settings (Pollack and Srinivasan, 2014). Antimicrobial
stewardship programs in hospitals are usually more developed than in outpatient
settings due to increased oversight by administration on hospital-wide practices, and
ease of collecting key outcome metrics, but there are examples of successful
stewardship interventions in ambulatory settings (Meeker et al., 2014; Pittenger et al.,
2015). Tracking process measures, such as adherence to guidelines for appropriate
antibiotic use and including indication for all prescriptions, and outcomes of interest,
such as C. difficile infections and antibiotic costs or days of therapy, are useful for
assessing the success of the program.
Measurement of antibiotic use with feedback to prescribers comparing them to their
peers is an effective approach for improving prescribing, but requires electronic
infrastructure not available in many settings. Various systems to measure human
antibiotic use exist but are fragmented and incomplete, such as CDC’s National
Healthcare Safety Network (NHSN) Antibiotic Use module, Intercontinental Marketing
Services (IMS) Health’s Xponent database, “all-payer-claims” databases, and electronic
health record data mining programs. None of these is currently able to provide a
comprehensive measurement of human antibiotic use in the US. In Washington, the
Department of Health has promoted CDC’s NHSN Antibiotic Use module, a system to
allow hospitals to electronically measure and report antibiotic use, but since this
program requires costly technological upgrades and expertise, state progress has been
limited to date. A statewide Washington all-payer-claims database is in development Antimicrobial
that will be useful for assessing outpatient antibiotic prescribing. Proprietary systems stewardship
such as IMP Xponent can provide prescribing data for a fee. Any widespread antibiotic
use measurement requires a high level of financial and human resources, therefore state
and federal mandates with financial support may be necessary in order to achieve
broad measurement.
121
Antimicrobial stewardship in companion animal practice
Surveys indicate that small animal veterinarians are increasingly concerned about AR.
(American Veterinary Medical Association Task Force for Antimicrobial Stewardship
in Companion Animal Practice, 2015) yet in companion animal practice, as in outpatient
human health care, there is little infrastructure to support antibiotic stewardship. In the
EU, 37 percent of pharmaceuticals sold are for use in companion animals (Guardabassi
et al., 2004), but in the USA there is no system for accurately measuring the proportion
of antibiotics sold for use in companion animals. FDA estimates 80 percent of
antibiotics sold in the USA are for use in animals, but this proportion includes both
companion animals as well as animals raised for food (Food and Drug Administration
(FDA), 2015). At Washington State University Veterinary Teaching Hospital, an
antimicrobial policy and oversight group performs stewardship for the teaching
hospital, but there is limited communication between academic and community
veterinarians. Available education and training resources for stewardship include US
Department of Agriculture (USDA) Veterinary Accreditation Training Modules and the
Antimicrobial Resistance Learning Site for Veterinarians. A structured guide for
implementing a stewardship program in a veterinary practice or hospital similar to
“core elements” for stewardship for human medicine has not been developed or
promulgated, however, the American Veterinary Medicine Association has produced
educational guidance on judicious therapeutic use of antibiotics to educate
veterinarians about appropriate use of antibiotics (www.avma.org/KB/Policies/Pages/
Judicious-Therapeutic-Use-of-Antimicrobials.aspx), and has convened a task force to
develop practice guidelines for implementing antimicrobial stewardship in companion
animal practice. Our Washington One Health group will be using results of the
veterinarian survey described earlier to guide educational outreach on stewardship for
veterinarians that, if well received, can be shared nationally.

Antimicrobial stewardship in livestock and animal agriculture

In animal agriculture, antibiotic treatment and control uses are most amenable to
stewardship interventions, similar to human and companion animal practices that focus
on the “4 Ds.” However, stewardship in food-animal agriculture presents three special
challenges not seen in human and companion animal sectors: antibiotics can frequently
be purchased and dispensed without a prescription; antibiotics are often used sub-
therapeutically for prevention and non-therapeutically for growth promotion; and some
food animal producers and veterinarians view efforts to reduce antibiotic use as a
potential threat to timely attention to animal welfare, affordability of meat, reliability of
the supply chain, and profits. Concern about widespread use of antibiotics in animal
agriculture and associated risk of resistance has prompted actions at the federal level. In
2007, USDA recommended certain farm management practices that can reduce the need
for antibiotics such as use of vaccines, probiotics, immune enhancers, proper nutrition,
and diet with adequate trace minerals, and improved operation procedures, such as
IJHG buying animals from herds with higher health status, pre-arrival testing of animals, use
21,3 of quarantine facilities, and elimination of contaminated feed and water (US Department
of Agriculture, 2007). In Washington, veterinarians associated with the Washington State
University work through the Cooperative Extension service to advise farmers about the
use of antibiotics but uptake by farms is voluntary.
In the past few years, the FDA issued new rules to increase veterinary oversight of
122 medically important antibiotics used in animal agriculture and promote judicious use of
these drugs by limiting use to treatment, control, and prevention of disease through
FDA Guidance for Industry No. 209 and No. 213, and changes to the VFD (FDA, 2013).
These mandates were structured with voluntary phase-in periods, allowing time for
pharmaceutical companies to change label indications and for industry to adjust
animal husbandry practices. Although antibiotics are currently available over-the-
counter for administration in animal feed products and water, mandatory changes in
2017 will require a veterinary directive for any antibiotics administered in food and
water. There is hope that these new requirements will result in increased veterinary
oversight for use of therapeutic antibiotics. Some proponents of strict regulation on
antibiotic use in animal agriculture, however, are concerned that antibiotics previously
used for growth promotion may subsequently be used, under veterinarian prescription,
for prevention purposes (Pew Charitable Trusts, 2014). Continued tracking of antibiotic
sales for use in food animals (FDA, 2015) will provide estimates as to whether guidance
No. 213 is successful in reducing the total mass of antibiotics used in animals. In 2016,
FDA is also providing new research funding to track antibiotic use in animal
agriculture after the mandatory changes are implemented.
Several states have undertaken assessments of knowledge, attitudes, and practices
about antibiotic use in food animal production. Larger food animal operations more
frequently followed written antibiotic use protocols, sought veterinarian consultation,
maintained better record keeping, and demonstrated a greater understanding of
biosecurity risks (Hoe and Ruegg, 2006; Raymond et al., 2006). In Washington,
veterinarians associated with the Washington State University provide educational
programs for veterinarians, farmers and farm workers on the development and risks of
AMR and alternatives to antibiotics, but participation by farms is voluntary.

Examples from other regions

Examining other state and international examples of restrictions on antibiotic use in
animal agriculture provide case studies that may inform future actions. A 2015 California
law, Senate Bill 27, bans all growth promotion uses of antibiotics and requires all
medically important antibiotics (as defined by FDA) be given only with a veterinary
prescription (California Legislative Information, 2015). The law also mandates monitoring
antibiotic use and resistance, and requires development and provision of guidance to
farmers on optimal use of antibiotics for food animal production. Denmark and Europe
provide opportunities to compare antibiotic use in food animals in comparable
high-income countries. Denmark halved antibiotic use in the pork industry between 1992
and 2008 by banning antibiotic growth promoters yet increased swine production by
47 percent, while remaining competitive with neighboring countries that did not restrict
antibiotic use in pigs (Cogliani et al., 2011). However, the Danish annual report on use of
antimicrobial agents and occurrence of resistance in food animals, food and humans,
indicates that in recent years therapeutic use of antibiotics has increased more rapidly
than herd size, suggesting a need to increase therapeutic use as non-therapeutic use
decreases (Danish Integrated Antimicrobial Resistance Monitoring and Research
Programme, 2014). Subsequent to Denmark’s ban on antibiotic growth promoters, the EU Antimicrobial
dictated an EU-wide ban on these growth promoters in 2005. Despite the ban, there is still stewardship
a wide range in antibiotic use in animal agriculture in the four largest pork producing
countries in Europe, Denmark, France, Germany, and Spain, where overall use in animals
varies from 44 mg/population control unit in Denmark to 317 mg/kg in Spain (European
Medicines Agency, 2015). Longitudinal study of the California and European experiences
will be instructive for tracking resistance in relation to antibiotic use. 123
Animal agriculture stakeholders often cite concerns about restrictions on antibiotic
use potentially causing increases in meat price. The economics of antibiotic use in US
livestock agriculture production was recently reviewed by USDA (Sneeringer et al.,
2015). The report details two important findings. First, antibiotics for growth
promotion are used widely in US livestock; in 2009, 40 percent of hogs received
antibiotic growth promoters as did 75 percent of cattle in feedlots with more than 1,000
head. Second, production uses of antibiotics may occur in two different structures:
vertical integration in which a single large business entity dictates and regulates
production conditions over the entire course of the animal’s life, and smaller operations
that focus only on one life stage. Vertical integration, with centralized oversight and
fewer decision-makers, provides more opportunity for systematically controlling how
antibiotics are used over the entire life course. According to USDA, use of antibiotics
for purposes other than disease treatment (i.e. for control, prevention, and production)
is associated with only a 1-3 percent increase in productivity, and restrictions on
production uses of antibiotics would result in less than 1 percent increase in wholesale
price and even smaller increases in retail prices (Sneeringer et al., 2015).
From a stewardship perspective, preventive uses may be minimized by reducing
physiologic stress to animals to keep them healthier, for example, by improving animal
husbandry practices, later weaning, reduced density of herds, improved hygiene,
rerouting air flow, and raising disease resistant breeds (European Commission, 2013b).
These interventions may be financially costly and may increase the price of meat but,
to date, no one has clearly evaluated the hidden costs related to the contribution of
animal agriculture to AR and thus the tradeoffs remain undefined. In 2015, only
approximately $11 million was available in funding for competitive extramural funding
for the 24 US veterinary colleges for research on animal health (Peter Johnson, personal
communication). Greater investments in research on animal health have potential to
substantially improve knowledge in this important area.
Recent announcements by McDonalds, Subway, Chicka-Fil-A, Panera, and Chipotle
that they will expand use of meat raised without antibiotics important to human
medicine indicate that the marketplace is responsive to consumer demands for
reducing antibiotic use in animal agriculture. Time will tell how completely these
companies can meet their pledges. An essential step is to clearly define and validate
label claims, such as “no non-therapeutic use,” “no production use,” or “no antibiotics
ever” to allow verification that actions live up to promises. Improved transparency
about how and how much antibiotics are used, how blanket restrictions on use
adversely affect animal welfare, and how variations in use affect animal safety, meat
availability, and prices, may allow consumers to make more informed decisions about
food purchases. The combination of regulation and marketplace demands may result
in significant changes over the coming years. The National Institute of Animal
Agriculture is acknowledging the changing environment by convening annual
meetings since 2011 that address scientific and production concerns regarding
antibiotic use (www.animalagriculture.org/WhitePapers).
IJHG Surveillance and data integration workgroup
21,3 The One Health Surveillance and Data Integration workgroup is a counterpart to
the One Health Antimicrobial Stewardship workgroup. Its task is to develop an
integrated database for tracking resistance data from humans, animals, and the
environment in Washington State. The group is compiling antimicrobial resistance
data from regional isolates, including: human and animal enteric pathogens from the
124 National Antibiotic Resistance Monitoring System; human and animal clinical
isolates from local microbiology labs; isolates from environmental sources such as
soil and water; and indicator species. The goal of the Washington One Health
Database of Antibiotic Resistance is to provide an ongoing local data source to
detect new trends in resistance and attempt to assess the impact of antimicrobial
stewardship efforts across human and animal and environmental sectors in the
region. In creating and analyzing such data, the database project will explore
comparability of human, animal, and environmental resistance patterns. To
encourage collaboration and ensure correct interpretation of results, the Washington
One Health Steering Committee will oversee data use, analyses and dissemination of
results from the database.

Summary
In summary, AR is increasing due to widespread use of antibiotics, and transmission of
resistant organisms in healthcare settings, in the community, via travel, and from food.
International, national and state efforts are underway to combat AR. In this paper, we
have described progress to date in Washington State to address this challenge from a
one health perspective. Our One Health committee and workgroups have succeeded in
convening key subject matter experts from the human, animal and environmental
health sectors to learn, strategize, and act to combat AR. We have chosen to focus
initially on increasing understanding of the current state of AR in Washington and
trends over time; minimizing transmission of resistant organisms; and improving use
of antibiotics in all sectors. Engaging food animal producers to learn and work with us
is an important next step.
As Lord Kelvin said, “If you cannot measure it, you cannot improve it.”
In all sectors, accurate measurement of antibiotic use is important to allow
evaluation of the effectiveness of stewardship interventions and to assess
correlation between antibiotic use and resistance surveillance data. In animal
agriculture, more granular measurement of antibiotic administration than that
provided by the FDA antibiotic sales data may allow increased understanding of
how changing antibiotic use affects animal health and production costs. Current US
capabilities to measure antibiotic use are deficient, especially when compared
to continent-wide surveillance of antibiotic use and bacterial resistance by the
European Centre for Disease Prevention and Control. With new funding for
combating AR efforts in the USA, there is potential for improving measurement of
antibiotic use in human medicine (both acute care and ambulatory settings),
veterinary medicine and agriculture. Additional federal support for implementing
national antibiotic use measurement in both acute care and ambulatory settings
would be extremely helpful since there is a need to both develop and sustain such
tracking systems.
Additional funding for research on resistance is needed to address other knowledge
gaps and identify how to best focus limited resources. Critical research opportunities
include: animal management strategies and their effect on animal health; source and Antimicrobial
quantity of environmental transmission of resistant strains; and quantification of type stewardship
and duration of antibiotics and AR genes in the environment, among others. We hope
that a description of our efforts can offer a model to other states that choose to engage
in similar work and may provide stimulus for national and international collaboration
to improve antibiotic use and minimize AR.
125
References
American Veterinary Medical Association Task Force for Antimicrobial Stewardship in
Companion Animal Practice (2015), “Understanding companion animal practitioners’
attitudes toward antimicrobial stewardship”, Journal of the American Veterinary Medical
Association, Vol. 247 No. 8, pp. 883-884.
Andersson, D.I. and Hughes, D. (2014), “Microbiological effects of sublethal levels of antibiotics”,
Nature Reviews Microbiology, Vol. 12 No. 7, pp. 465-478.
Arp, D. (2012), “Pharmacy options for veterinary practices”, Veterinary Practice News, June 26,
available at: www.veterinarypracticenews.com/June-2012/Pharmacy-Options-For-
Veterinary-Practices/ (accessed March 5, 2016).
Barlam, T.F., Cosgrove, S.E., Abbo, L.M., MacDougall, C., Schuetz, A.N., Septimus, E.J., Srinivasan, A.,
Dellit, T.H., Falck-Ytter, Y.T., Fishman, N.O., Hamilton, C.W., Jenkins, T.C., Lipsett, P.N.,
Malani, P.N. and May, L.S. (2016), “Implementing an antibiotic stewardship program:
guidelines by the infectious diseases society of America and the society for healthcare
epidemiology of America”, Clinical Infectious Diseases, Vol. 62 No. 10, pp. 1197-1202.
Blanco, G., Lemus, J.A. and Grande, J. (2009), “Microbial pollution in wildlife: linking agricultural
manuring and bacterial antibiotic resistance in red-billed choughs”, Environmental
Research, Vol. 109 No. 4, pp. 405-412.
Blazquez, J., Oliver, A. and Gomez-Gomez, J.-M. (2001), “Mutation and evolution of antibiotic
resistance: antibiotics as promoters of antibiotic resistance”, Current Drug Targets, Vol. 3
No. 4, pp. 345-349.
California Legislative Information (2015), “Livestock: use of antimicrobial drugs”, Senate Bill
No. 27, available at: https://leginfo.legislature.ca.gov/faces/billNavClient.xhtml?bill_
id¼201520160SB27 (accessed March 8, 2016).
Centers for Disease Control and Prevention (2013), “Antibiotic resistance threats in the United
States, 2013”, US Centers for Disease Control and Prevention, Atlanta, GA.
Cogliani, C., Goossens, H. and Greko, C. (2011), “Restricting antimicrobial use in food animals:
lessons from Europe banning nonessential antibiotic uses in food animals is intended to
reduce pools of resistance genes”, Microbe, Vol. 6 No. 6, pp. 274-279.
Council of State and Territorial Epidemiologists (2015), “Position statement 15-ID-02:
recommendations for strengthening antimicrobial stewardship in veterinary medicine
and animal agriculture”, available at: http://c.ymcdn.com/sites/www.cste.org/resource/
resmgr/2015PS/2015PSFinal/15-ID-02.pdf (accessed May 26, 2016).
Cox, G.I. and Wright, G.D. (2013), “Intrinsic antibiotic resistance: mechanisms, origins, challenges
and solutions”, International Journal of Medical Microbiology, Vol. 303 Nos 6-7, pp. 287-292.
Danish Integrated Antimicrobial Resistance Monitoring and Research Programme (2014), “Use of
antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food
animals, food and humans in Denmark”, Statens Serum Institut National Veterinary
Institute, Technical University of Denmark National Food Institute, Kongens Lyngby,
September 2015.
IJHG Davey, P., Brown, E., Fenelon, L., Finch, R., Gould, I., Holmes, A., Ramsay, C., Taylor, E.,
Wiffen, P. and Wilcox, M. (2006), “Systematic review of antimicrobial drug prescribing in
21,3 hospitals”, Emerging Infectious Diseases, Vol. 12 No. 2, pp. 211-216.
Dipeolu, M.A. and Alonge, D.O. (2002), “Residues of streptomycin antibiotic in meat
sold for human consumption in some states of SW Nigeria”, Archivos de Zootecnia,
Vol. 51, pp. 477-480.
126 Dutil, L., Irwin, R., Finley, R., Ng, L.K., Avery, B., Bourgault, A.M., Cole, L., Daignault, D.,
Desruisseau, A., Demczuk, W., Hoand, L., Horsman, G.B., Ismail, J., Jamieson, F.,
Pacagnella, A. and Pillai, D.R. (2010), “Ceftiofur resistance in Salmonella enterica serovar
Heidelberg from chicken meat and humans, Canada”, Emerging Infectious Diseases, Vol. 16
No. 1, pp. 48-54.
Enne, V.I. (2010), “Reducing antimicrobial resistance in the community by restricting
prescribing: can it be done?”, Journal of Antimicrobial Chemotherapy, Vol. 65 No. 2,
pp. 179-182.
European Commission (2013a), “Evaluation of CAP measures for the apiculture sector”,
Agriculture and Rural Development DG-Final Report 2013, Brussels, July, available at:
http://ec.europa.eu/agriculture/evaluation/market-and-income-reports/2013/apiculture/
fulltext_en.pdf (accessed May 16, 2016).
European Commission (2013b), “EIP-AGRI focus group reducing antibiotic use in pig
farming final report 2013”, available at: http://ec.europa.eu/eip/agriculture/sites/
agri-eip/files/eip-agri_fg3_pig_antibiotics_final_report_2014_en.pdf (accessed Feburary
11, 2016).
European Medicines Agency (2015), “Sales of veterinary antimicrobial agents in 26 EU/EEA
countries in 2013 Fifth ESVAC report”, available at: www.ema.europa.eu/docs/en_GB/
document_library/Report/2015/10/WC500195687.pdf (accessed Feb 19, 2016).
Fey, P.D., Safranek, T.J. and Rupp, M.E. (2000), “Ceftriaxone-resistant salmonella infection
acquired by a child from cattle”, New England Journal of Medicine, Vol. 342 No. 17,
pp. 1242-1249.
Fick, J., Soderstrom, H., Lindberg, R.H., Phan, C., Tysklind, M. and Larsson, D.G. (2009),
“Contamination of surface, ground, and drinking water from pharmaceutical production”,
Environmental Toxicology and Chemistry, Vol. 28 No. 12, pp. 2522-2527.
Fleming-Dutra, K.E., Hersh, A.L., Shapiro, D.J., Bartoces, M., Enns, E.A., File, T.M., Finkelstein, J.A.,
Gerber, J.S., Hyun, D.Y., Linder, J.A., Lynfield, R., Margolis, D.J., May, L.S., Merenstein, D.,
Metlay, J.P., Newland, J.G., Piccirillo, J.F., Roberts, R.M., Sanchez, G.V., Suda, K.J.
et al. (2016), “Prevalence of inappropriate antibiotic prescriptions among US ambulatory
care visits, 2010-2011”, Journal of the American Medical Association, Vol. 315 No. 17,
pp. 1864-1873.
Food and Agriculture Organization of the United Nations (2015), “Global aquaculture production
statistics database updated to 2013 summary information”, available at: www.fao.org/3/
a-i4899e.pdf (accessed March 5, 2016).
Food and Drug Administration (FDA) (2013), “Guidance for industry on new animal drugs and new
animal drug combination products administered in or on medicated feed or drinking water of
food-producing animals: recommendations for drug sponsors for voluntarily aligning
product use conditions with guidance for industry No. 209”, available at: www.
federalregister.gov/articles/2013/12/12/2013-29697/guidance-for-industry-on-new-animal-
drugs-and-new-animal-drug-combination-products-administered-in (accessed May 18, 2016).
Food and Drug Administration (FDA) (2015), “2013 Summary report on antimicrobials
sold or distributed for use in food-producing animals”, Department of Health and Human
Services, April.
Fridkin, S., Baggs, J., Fagan, R., Magill, S., Pollack, L., Malpiedi, P., Slayton, R., Khader, K., Antimicrobial
Rubin, M.A., Jones, M., Samore, M.H., Dumyati, G., Dodds-Ashley, E., Meek, J.,
Yousey-Hindes, K., Jernigan, J., Shehab, N., et al. (2014), “Vital signs: improving antibiotic use
stewardship
among hospitalized patients”, Morbidity and Mortality Weekly Report, Vol. 63 No. 9,
pp. 194-200.
Guardabassi, L., Schwarz, S. and Lloyd, D.H. (2004), “Pet animals as reservoirs of
antimicrobial-resistant bacteria”, Journal of Antimicrobial Chemotherapy, Vol. 54 No. 2, 127
pp. 321-332.
Harrison, E.M., Weinert, L.A., Holden, M.T., Welch, J.J., Wilson, K., Morgan, F.J., Loeffler, A.,
Boag, A.K., Peacock, S.J., Paterson, G.K., Waller, A.S., Parkhill, J. and Holmes, M.A. (2014),
“A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates
in humans and companion animals”, mBio, Vol. 5 No. 3, pp. e00985-13.
Harrison, E.M., Paterson, G.K., Holden, M.T., Larsen, J., Stegger, M., Larsen, A.R., Petersen, A.,
Skov, R.L., Christiansen, J.M., Bak Zeuthen, A., Heltberg, O., Harris, S.R., Sadoks, R.N.,
Parkhill, S.J. and Holmes, M.A. (2013), “Whole genome sequencing identifies zoonotic
transmission of MRSA isolates with the novel mecA homologue mecC”, EMBO Molecular
Medicine, Vol. 5 No. 4, pp. 509-515.
Hecker, M.T., Aron, D.C., Patel, N.P., Lehmann, M.K. and donskey, C.J. (2003), “Unnecessary
use of antimicrobials in hospitalized patients: current patterns of misuse with an emphasis
on the antianaerobic spectrum of activity”, Archives of Internal Medicine, Vol. 163 No. 8,
pp. 972-978.
Hoe, F.G. and Ruegg, P.L. (2006), “Opinions and practices of Wisconsin dairy producers
about biosecurity and animal well-being”, Journal of Dairy Science, Vol. 89 No. 6,
pp. 2297-2308.
Hooper, C.D. and Jacoby, G.A. (2015), “Mechanisms of drug resistance: quinolone resistance”,
Annals of the New York Academy of Sciences, Vol. 1354, pp. 12-13.
Huddleston, J.R. (2014), “Horizontal gene transfer in the human gastrointestinal tract:
potential spread of antibiotic resistance genes”, Infection and Drug Resistance, Vol. 20
No. 7, pp. 167-176.
Joseph, J. and Rodvold, K.A. (2008), “The role of carbapenems in the treatment of severe
nosocomial respiratory tract infections”, Expert Opinion on Pharmacotherapy, Vol. 9 No. 4,
pp. 561-575.
King, L. (2014), “Antibiotic use and resistance: moving forward through shared stewardship”,
white paper-Antibiotic Use and Resistance: Moving Forward Through Shared Stewardship
from proceedings of the National Institute of Animal Agriculture Antibiotics Symposium,
Atlanta, GA, November 12-14, p. 9.
Lazarus, B., Paterson, D.L., Mollinger, J.L. and Rogers, B.A. (2015), “Do human extraintestinal
Escherichia coli infections resistant to expanded-spectrum cephalosporins originate from
food-producing animals? A systematic review”, Clinical Infectious Diseases, Vol. 60 No. 3,
pp. 439-452.
Le Devendec, L., Bouder, A., Dheilly, A., Hellard, G. and Kemph, I. (2011), “Persistence and spread
of qnr, extended-spectrum beta-lactamase, and ampC resistance genes in the digestive tract
of chicken”, Microbial Drug Resistance, Vol. 17 No. 1, pp. 129-134.
Levy, S.B., FitzGerald, G.B. and Macone, A.B. (1976), “Changes in intestinal flora of farm
personnel after introduction of a tetracycline-supplemented feed on a farm”, New England
Journal of Medicine, Vol. 295 No. 11, pp. 583-588.
McManus, P.S. (2014), “Does a drop in the bucket make a splash? Assessing the impact of
antibiotic use on plants”, Current Opinion in Microbiology, Vol. 19, pp. 76-82.
IJHG Magill, S.S., Edwards, J.R., Bamberg, W., Beldavs, Z.G., Dumyati, G., Kainer, M.A., Lynfield, R.,
Maloney, M., McAllister-Hollod, L., Nadle, J., Ray, S.M., Thompson, D.L., Wilson, L.E. and
21,3 Fridkin, S.K. (2014), “Multistate point-prevalence survey of health care–associated infections”,
New England Journal of Medicine, Vol. 370 No. 13, pp. 1198-1208.
Manges, A. (2016), “Escherichia coli and UTI: the role of poultry-meat”, Clinical Microbiology and
Infection, Vol. 22 No. 2, pp. 122-129.
128 Meeker, D., Knight, T.K., Friedberg, M.W., Linder, J.A., Goldstein, N.J., Fox, C.R., Rothfeld, A. and
Doctor, J.N. (2014), “Nudging guideline-concordant antibiotic prescribing: a randomized
clinical trial”, JAMA Internal Medicine, Vol. 174 No. 3, pp. 425-431.
Nordmann, P., Naas, T. and Poirel, L. (2011), “Global spread of carbapenemase-producing
Enterobacteriaceae”, Emerging Infectious Diseases, Vol. 17 No. 10, pp. 1791-1798.
Ornstein, C., Weber, T. and Nguyen, D. (2011), “Piercing the veil, more drug companies
reveal payments to doctors”, ProPublica, September 7, available at: www.propublica.org/
article/piercing-the-veil-more-drug-companies-reveal-payments-to-doctors (accessed March
5, 2016).
Pew Charitable Trusts (2014), “Gaps in FDA’s antibiotics policy”, Issue Brief Pew
Charitable Trusts, Washington, DC, November 30, available at: www.pewtrusts.org/en/
research-and-analysis/issue-briefs/2014/11/gaps-in-fdas-antibiotics-policy (accessed
February 11, 2016).
Pittenger, K., Williams, B.L., Mecklenburg, R.S. and Blackmore, C.C. (2015), “Improving acute
respiratory infection care through nurse phone care and academic detailing of physicians”,
Journal of the American Board of Family Medicine, Vol. 28 No. 2, pp. 195-204.
Pollack, L.A. and Srinivasan, A. (2014), “Core elements of hospital antibiotic stewardship
programs from the centers for disease control and prevention”, Clinical Infectious Diseases,
Vol. 59 No. S3, pp. S97-S100.
Price, L.B., Stegger, M., Hasman, H., Aziz, M., Larsen, J., Andersen, P.S., Pearson, T., Waters, A.E.,
Foster, J.T., Schupp, J. Gillece, J., Driebe, E., Liu, C.M., Springer, B., Zdovc, I., Battisti, A. and
Franco (2012), “Staphylococcus aureus CC398: host adaptation and emergence of methicillin
resistance in livestock”, mBio, Vol. 3 No. 1, pp. e00305-e00311.
Rafee, Y., Abdel-Haq, N., Asmar, B., Salimnia, T., Pharm, C.V., Rybak Pharm, M.J. and Amjad, M.
(2012), “Increased prevalence of methicillin-resistant Staphylococcus aureus nasal
colonization in household contacts of children with community acquired disease”, BMC
Infectious Diseases, Vol. 12 No. 45, pp. 1-7.
Raymond, M.J., Wohrle, R.D. and Call, D.R. (2006), “Assessment and promotion of judicious
antibiotic use on dairy farms in Washington State”, Journal of Dairy Science, Vol. 89 No. 8,
pp. 3228-3240.
Singer, R. (2015), “Urinary tract infections attributed to diverse ExPEC strains in food animals:
evidence and data gaps”, Frontiers in Microbiology, Vol. 6 No. 28, pp. 1-9.
Sneeringer, S., MacDonald, J., Key, N., McBride, W. and Mathews, K. (2015), “Economics
of antibiotic use in US livestock production”, Economic Research Report No. 200,
US Department of Agriculture, Economic Research Service, Washington, DC,
November.
Stockwell, V.O. and Duffy, B. (2012), “Use of antibiotics in plant agriculture”, World Organisation
for Animal Health, OIE Scientific and Technical Review; Special Issue: Antimicrobial
Resistance in Animal and Public Health, Vol. 31 No. 1, pp. 199-210.
Subbiah, M., Mitchell, S., Ullman, J. and Call, D.R. (2011), “Beta-lactams and florfenicol antibiotics
remain bioactive in soils while ciprofloxacin, neomycin, and tetracycline are neutralized”,
Applied and Environmental Microbiology, Vol. 77 No. 20, pp. 7255-7260.
US Department of Agriculture (2007), “Antimicrobial resistance issues in animal agriculture”, Antimicrobial
available at: www.aphis.usda.gov/animal_health/emergingissues/downloads/antiresist
2007update.pdf (accessed March 7, 2016).
stewardship
van Duijkeren, E., Wolfhagen, M.J., Box, A.T.A., Heck, M.E., Wannet, W.J. and Fluit, A.C. (2004),
“Human-to-dog transmission of methicillin-resistant Staphylococcus aureus”, Emerging
Infectious Diseases, Vol. 10 No. 12, pp. 2235-2237.
Vieira, A.R., Collignon, P., Aarestrup, F.M., McEwen, S.A., Hendriksen, R.S., Hald, T. and 129
Wegener, H.C. (2011), “Association between antimicrobial resistance in Escherichia coli isolates
from food animals and blood stream isolates from humans in Europe: an ecological study”,
Foodborne Pathogens and Disease, Vol. 8 No. 12, pp. 1295-1301.
Washington State Department of Health (2015), “Open letter to Washington State on combating
antibiotic resistant bacteria”, available at: www.doh.wa.gov/Portals/1/Documents/5410/
OneHealthAMSLetter.pdf (accessed May 26, 2016).
Washington State Veterinary Medical Association (2015), “Judicious use of antimicrobials
general practice principles”, available at: http://wsvma.org/wp-content/uploads/2014/11/
Judicious-Use-of-Antimicrobials-Brochure.pdf (accessed on March 7, 2016).
World Health Organization (2012), The Evolving Threat of Antimicrobial Resistance: Options for
Action, ISBN:9789241503181, World Health Organization, Geneva.
Youngquist, C.P., Liu, J., Orfe, L.H., Jones, S.S. and Call, D.R. (2014), “Ciprofloxacin residues in
municipal biosolids compost do not selectively enrich populations of resistant bacteria”,
Applied and Environmental Microbiology, Vol. 80 No. 24, pp. 7521-7526.

Author Affiliations
Marisa Anne D’Angeli, Department of Communicable Disease Epidemiology, Washington
State Department of Health, Shoreline, Washington, USA
Joe B. Baker, Animal Services Division, Washington State Department of Health, Olympia,
Washington, USA
Douglas R. Call and Margaret A. Davis, Paul G. Allen School for Global Animal Health,
Washington State University, Pullman, Washington, USA
Kelly J. Kauber, Department of Communicable Disease Epidemiology, Washington State
Department of Health, Shoreline, Washington, USA
Uma Malhotra, Department of Infectious Diseases, Virginia Mason Hospital and Seattle
Medical Center, Seattle, Washington, USA
Gregory T. Matsuura, Department of Infection Prevention/Antibiotic Stewardship, Yakima
Valley Memorial Hospital, Yakima, USA
Dale A. Moore, Department of Veterinary Clinical Sciences, College of Veterinary Medicine,
Washington State University, Pullman, Washington, USA
Chris Porter, United Advanced Registered Nurse Practitioners of Washington, Seattle,
Washington, USA
Paul Pottinger, Allergy and Infectious Disease Division, University of Washington Medical
Center, Seattle, Washington, USA
Virginia Stockwell, Agricultural Research Service, Horticultural Crops Research Unit, United
States Department of Agriculture, Corvallis, Oregon, USA
Carol Wagner, Patient Safety Program, Washington State Hospital Association, Seattle,
Washington, USA
Ron Wohrle, Zoonotic Disease Program, Office of Environmental Public Health Sciences,
Washington State Department of Health, Olympia, Washington, USA
IJHG Jonathan Yoder, School of Economic Sciences, Washington State University, Pullman,
Washington, USA and Paul G. Allen School for Global Animal Health, Washington State
21,3 University, Pullman, Washington, USA
Leah Hampson Yoke, Vaccine and Infectious Disease Division, Fred Hutchinson Cancer
Research Center, Seattle, Washington, USA and Allergy and Infectious Disease Division,
School of Medicine, University of Washington, Seattle, Washington, USA, and
130 Peter Rabinowitz, Center for One Health Research, Department of Environmental and
Occupational Health, University of Washington, Seattle, Washington, USA

Corresponding author
Marisa Anne D’Angeli can be contacted at: [email protected]

For instructions on how to order reprints of this article, please visit our website:
www.emeraldgrouppublishing.com/licensing/reprints.htm
Or contact us for further details: [email protected]
This article has been cited by:

1. David Birnbaum Applied Epidemiology, North Saanich, Canada Michael Decker Department of
Health Policy, Vanderbilt University, Baxter, Tennessee, USA . 2016. Halfway to salvation, or
halfway to hell?. International Journal of Health Governance 21:3, 106-113. [Abstract] [Full Text]
[PDF]
2. Fiona MacVane Phipps University of Salford, Salford, UK . 2016. IJHG review. International
Journal of Health Governance 21:3, 194-199. [Abstract] [Full Text] [PDF]