The large and expanding use of antimicrobials in livestock, a consequence of growing
global demand for animal protein, is of considerable concern in light of the threat
of antimicrobial resistance (AMR). Use of antimicrobials in animals has been linked
to drug-resistant infections in animals (
1
) and humans (
2
). In September 2016, the United Nations (UN) General Assembly recognized the inappropriate
use of antimicrobials in animals as a leading cause of rising AMR. In September 2018,
the interagency group established by the UN Secretary General will report on progress
in the global response to AMR, including antimicrobial consumption in animals. We
provide a baseline to monitor efforts to reduce antimicrobial use and assess how three
global policies might curb antimicrobial consumption in food animal production: (i)
enforcing global regulations to cap antimicrobial use, (ii) adherence to nutritional
guidelines leading to reduced meat consumption, and (iii) imposing a global user fee
on veterinary antimicrobial use.
The rise of AMR in zoonotic pathogens, including to last-resort drugs such as colistin
(
3
), is an important challenge for human medicine because it can lead to untreatable
infections. Evidence linking AMR between animals and humans is particularly strong
for common foodborne pathogens resistant to quinolones, such as Campylobacter spp.
and Salmonella spp. (
4
). AMR is also a threat to the livestock sector and thus to the livelihoods of millions
who raise animals for subsistence (
5
).
The primary driver for the accumulation of harmful resistance genes in the animal
reservoir is the large quantity of antimicrobials used in animal production (
6
). Antimicrobial use in livestock, which in many countries outweighs human consumption
(
7
), is primarily associated with the routine use of antimicrobials as growth promoters
or their inappropriate use as low-cost substitutes for hygiene measures that could
otherwise prevent infections in livestock.
In Europe, regulations have been the principal instrument to limit antimicrobial use
in animal production. In the United States, consumer preferences have driven companies
to reduce antimicrobial use in animals, although the impact on livestock rearing practices
is still nascent (
8
). Some European countries maintain highly productive livestock sectors while using
less than half the current global average amount of antimicrobial per kilogram of
animal (50 mg/kg). Therefore, this threshold has been proposed as a potential target
for global regulations on veterinary antimicrobial use (
9
). However, the impact that such policies would have on the global consumption of
antimicrobials has yet to be quantified.
A second solution to reduce antimicrobial consumption in animal production may be
to promote low-animal-protein diets: China has recently revised downward its nutritional
guidelines for meat intake to 40 to 70 g/day (
10
), which is approximately half the current consumption level in the country. If followed,
this measure could have an indirect but substantial impact on the global consumption
of veterinary antimicrobials. A third solution to cut antimicrobial use would be to
charge a user fee, paid by veterinary drug users, on sales of antimicrobials for nonhuman
use (
11
). This approach has recently received support from the World Bank (
12
) on the basis that the associated revenues could be injected into a global fund to
stimulate discovery of new antimicrobials and support efforts to preserve existing
drugs (
13
). Without further analysis, however, it is unclear whether a user fee policy could
achieve a meaningful reduction in the global consumption of veterinary antimicrobials,
let alone generate sufficient revenues to support improved livestock rearing practices
or the development of new drugs, vaccines, and diagnostics.
GLOBAL TRENDS
Veterinary antimicrobial sales volumes were obtained via public records for 38 countries
and self-governing dependencies and estimated for 190 more (supplementary materials).
In 2013, the global consumption of all antimicrobials in food animals was estimated
at 131,109 tons [95% confidence interval (CI) (100,812 to 190,492 tons)] and is projected
to reach 200,235 tons [95% CI (150,848 to 297,034 tons)] by 2030. Consumption levels
varied considerably between countries, ranging from 8 mg/population correction unit
(PCU) (a kilogram of animal product) in Norway to 318 mg/PCU in China (see fig. S1).
As the largest consumer of veterinary antimicrobials, both in relative (per PCU) and
in absolute terms, China has an important leadership role with regard to its response
to AMR and has already set precedents in phasing out drugs that are last resorts for
human infections but are still in use in Europe in animal husbandry.
In relative terms, humans and animals use comparable amounts of antimicrobials [118
mg/PCU and 133 mg/kg, respectively (
14
)], but given that the biomass of animals raised for food exceeds by far the biomass
of humans, new resistant mutations are more likely to arise in animals. Furthermore,
a central distinction between animals and humans is the purpose of antimicrobial use.
Unlike in humans, antimicrobial use in animals is primarily intended for growth promotion
and mass prophylaxis. These uses are often administered both through feed, directly
targeting the gut, and in low-dose patterns that promote the evolution of resistance
(
15
). These factors suggest that the food animal reservoir is a greater source of resistance
genes than humans. However, the subsequent spread of those genes to humans follows
complex pathways, and recent work has highlighted that curtailing antimicrobial use
in animals alone will not suffice to contain AMR in humans (
16
).
Pigs in cages, Quanzhou, China. As the largest consumer of veterinary antimicrobials,
China is critical for combating antimicrobial resistance (AMR).
GLOBAL SOLUTIONS
The use of antimicrobials in food animals could be reduced by 2030 between 9 and 80%
with effective policies compared with a business-as-usual target (BAU) of continued
growth of the livestock sector with current levels of antimicrobial use (see the graph).
This could be achieved either by reducing the quantity of antimicrobial used per animal
(targets 1 and 3) or the number of animals that we raise for food (target 2).
Regulations. A global regulation putting a cap of 50 mg of antimicrobials per PCU
per year, the current global average amount, could reduce total consumption by 64%
(target 1A). If only countries of the Organization for Economic Cooperation and Development
(OECD) and China were to adopt this regulation, the global consumption in 2030 would
already be reduced by 60% (target 1B). In the short term, target 1B may be preferred
because it would have substantial impact on global consumption without targeting vulnerable
farmers in low- and middle-income countries (LMICs) who rely on the ability to treat
livestock for subsistence (
17
). In some high-income countries, regulatory approaches have achieved substantial
reduction in antimicrobial use within a few years and at moderate costs. However,
in LMICs, the cost of setting up surveillance systems is a barrier to enforcement,
and our findings are contingent on enforceability.
Meat consumption. Limiting meat intake worldwide to 40 g/day—the equivalent of one
standard fast-food burger per person— could reduce global consumption of antimicrobials
in food animals by 66% (target 2A). This reduction is comparable with what could be
achieved through regulations targeting antimicrobial use (targets 1A and 1B). In comparison,
meat consumption in the United States currently averages 260 g/ day (OECD 2015). In
this context, and given increasing appetites for meat in emerging economies, it seems
unlikely that antimicrobial use in food animals could be reduced substantially through
voluntary adherence to such drastic changes in dietary habits. Under a more realistic
global cap of 165 g meat/day (projected EU average in 2030), global consumption of
antimicrobials could be reduced by 22% (target 2B). Reduced meat consumption could
thus have substantial benefits on AMR as well as other environmental and human health
issues.
User fees. Imposing a user fee of 50% of the current price on veterinary antimicrobials
could reduce global consumption by 31% (target 3C). More important, such a policy
would also generate yearly revenues between US$ 1.7 billion and 4.6 billion (Protocol
S4). In comparison, the level of investment necessary for the development of one new
antimicrobial compound is typically US$ 1 billion (
18
). Alternative rates of 10 or 100% for the user fee would reduce the global consumption
by 9 and 46%, generating revenues of US$ 0.4 billion to 1.2 billion and US$ 2.8 billion
to 7.5 billion, respectively. Concretely, the fee could be applied at the point of
manufacture or wholesale purchase for imported products. The advantages of this implementation
are twofold. First, given the limited number of drug manufacturers, enforcement would
require only limited resources. Second, manufacturers are more likely than veterinarians
to keep records of volumes traded, especially in countries where drugs are used without
prescription. However, because user fees could be passed on to individual farmers,
these could also have adverse effects if not accompanied by other measures to reduce
the need for antimicrobials in food production. Here, we identify that demand for
veterinary antimicrobials is on average more elastic in LMICs (Protocol S4), with
the notable exception of China, where demand was inelastic because of increased reliance
on antimicrobials for food production. LMICs could therefore be disproportionally
affected by a user fee.
COMPARISON AND LIMITATIONS
The solutions presented in this analysis are not mutually exclusive; if considered
in combinations, regulatory caps, user fees, and reductions in meat intake could potentially
reduce global consumption of antimicrobials in animals by up to 80%. However, implementation
of those policies should account for differences across income groups. We show that
a global user fee policy could circumvent the limitations inherent to regulatory approaches
while still achieving a meaningful reduction in antimicrobial use (31%).
Unlike regulations that may be virtually impossible to enforce in LMICs, a user fee
policy could be applied immediately, without waiting for costly surveillance networks
to put in place. In LMICs, large livestock producers could follow the example from
European countries, where drastic reductions in antimicrobial consumption could have
potential long-term benefits. In compensation for the reduction in antimicrobial use
in LMICs, major investments will be needed to improve farm hygiene and expand veterinary
services. We show that these could be partly financed with the revenues of the user
fee policy through a global fund. In parallel, national programs should also ensure
that antimicrobials used for treatment by smallholders remain affordable so that a
global user fee doesn’t become an obstacle for livestock- driven economic development.
In the long run, this transition to low antimicrobial use could benefit all countries:
Phasing out growth that promotes antimicrobials will likely have limited impact on
food production (
19
) but would reduce the risk of emergence of pathogens resistant to lastresort drugs
(
3
). Reducing antimicrobial use may also benefit LMICs to secure export markets where
customers express preferences for products obtained without antimicrobials (
8
) and restriction on antimicrobial use may apply as part of trade agreements.
Our findings are subject to limitations. For example, although more countries (including
LMICs) have reported sales of antimicrobials for this estimate compared with 2010
(
20
), information on sales broken down by species and by classes of compounds is still
limited. As a result, consumption in nonreporting countries can only be estimated
through extrapolations. In addition, available information on antimicrobial prices
prevents a more advanced economic analysis on the impact of user fees than presented
in this study. Unlike for human medicine, there is currently no global database (public
or private) on veterinary antimicrobial sales accessible to the public health community.
Although present data are limited, outlining current knowledge allows inferences to
be made about the relative impact of different policies to curb antimicrobial use.
Our findings suggest that imposing a user fee on veterinary antimicrobials is a plausible
policy option to achieve meaningful reductions in antimicrobial use in the short term
while simultaneously raising funds to improve farming practices that will benefit
the long-term viability of the livestock industry.
Antimicrobial consumption in food animals by 2030
Business as usual and intervention policies are shown. Revenue ranges are estimated
for different fee rates (TR) and price elasticities of demand (PED). For 3C, 3D, and
3E, PEDs are derived from time series of imports of veterinary antimicrobials in each
country (Protocol S4); the global average PED was -0.95. See supplementary materials
for discussions of uncertainty in all estimates shown in figures. PCU, population
correction unit.
Supplementary Material
Click here for additional data file.