Global trends in antimicrobial use in aquaculture

By: Daniel Schar, EiliY. Klein, Ramanan Laxminarayan, Marius Gilbert, and Thomas P. Van Boeckel *

Several countries have experienced dramatic reductions in antimicrobial use rates following the introduction of vaccination and improved management and husbandry programs, serving as important antimicrobial stewardship models.

Aquatic animals represent 17% of animal protein consumed globally, and for over 40% of the world’s population, fish contribute nearly 20% of per capita animal protein consumed. Aquaculture now accounts for nearly half of the global supply of fisheries products for human consumption.

Globally, rising demand for animal source nutrition is The levels and patterns of antimicrobial use in aquaculture globally remain largely undocumented, limiting application of targeted interventions and policies promoting sound antimicrobial stewardship in a high-growth industry.

This study presents an analysis of global antimicrobial consumption trends in aquaculture. The estimates presented here provide an initial foundation upon which future studies will be able to build and refine in directing iterative enhancements in antimicrobial stewardship policies being met with a transition to increasingly intensive animal production systems.

This transitional period is typically characterized by an emphasis on production volume that precedes the adoption of farm biosecurity, hygiene and management standards. In this context, nontherapeutic antimicrobial use may serve to increase growth and substitute for good animal husbandry practices.

“Compared with antimicrobial use in terrestrial food animal production, application of antimicrobials in aquaculture provides a potentially wider environmental exposure pathway for drug distribution through water with important ecosystem health implications.”

Antimicrobial residues in the aquatic environment alter the environmental microbiome and, consequently, ecosystem regulatory, provisioning and supporting capacities.

In addition to disease regulation, the aquatic environmental microbiome’s function in nutrient cycling, sustaining biodiversity, carbon sequestration, and freshwater availability remain important research inquiries.

The levels and patterns of antimicrobial use in aquaculture globally remain largely undocumented, limiting application of targeted interventions and policies promoting sound antimicrobial stewardship in a high-growth industry.

In this study we present an analysis of global antimicrobial consumption trends in aquaculture. The estimates presented here provide an initial foundation upon which future studies will be able to build and refine in directing iterative enhancements in antimicrobial stewardship policies.

Methods


Baseline antimicrobial consumption and projected growth through 2030 were calculated by application of species-specific antimicrobial use coefficients to current and projected aquaculture production by species.

We conducted a systematic review of peer-review and grey literature for antimicrobial use point prevalence surveys in aquaculture between 2000 and 2019, using three primary search term categories: “antimicrobial” (antimicrobial; antibiotic; veterinary medicine); “use” (use; usage; consumption; amount; quantity); and “aquaculture” (aquaculture; aquatic; fish; shellfish; marine; freshwater).

Aquaculture baseline and projections. Corresponding production statistics in 2017 by country, region, and for five species categories—catfish, shrimp, salmon, tilapia, and trout—were collected from FAO FishStat.

“In aquaculture, antimicrobials are primarily delivered through feed for both therapeutic and nontherapeutic use.”

For each country or region, the difference between the total production figure and the sum of the five species categories was assigned to a sixth category, “pooled.” The 2017–2027 compound annual growth rate generated projected production figures from 2028 to 2030 Uncertainty.

Mean antimicrobial use coefficients in mg kg-1 were calculated for each of the six species categories by calculating the mean of the log10 transformed speciesspecific use rates from the point prevalence surveys.

A sensitivity analysis was also performed to identify outliers. Antimicrobial use coefficients for each point prevalence survey were sequentially excluded from the calculation of the mean. The resultant mean coefficients were compared with the mean of the full list of surveys. A similar analysis was performed using mean coefficients by country.

Aggregate global consumption. Antimicrobial consumption from terrestrial food animals and base- line estimates from humans were obtained from Van Boeckel et al, and Klein et al, respectively. Consumption trends from terrestrial food animal species were adjusted to reflect revised animal biomass projections from 2017 to 2030.

Results

Global antimicrobial consumption in aquaculture in 2017 was estimated at 10,259 tons. The four countries with the largest share of antimicrobial consumption in 2017 were all in the Asia–Pacific region: China (57.9%), India (11.3%), Indonesia (8.6%), and Vietnam (5%). These countries are projected to remain the largest consumers of antimicrobials in 2030.

The countries with the largest projected relative increase in consumption between 2017 and 2030 were Brazil (94%), Saudi Arabia (77%), Australia (61%), Russia (59%) and Indonesia (55%) by species groups. Five species groups were established in our study: catfish, shrimp, salmon, tilapia, and trout. Among the individual species groups, 8.3% of global antimicrobial consumption was attributable to catfish, 3.4% to tilapia, 2.7% to shrimp, 0.8% to trout, and 0.7% to salmon.

The relative proportion of each species group was stable through 2030. The influence of production system on antimicrobial use was assessed using a one-way analysis of variance (ANOVA) test, which revealed no significant association (P = 0.543) between production system intensity and use when comparing intensive, semi-intensive, and mixed systems.


Trends by antimicrobial class

Globally, the most commonly used classes of antimicrobials were, by frequency of use, quinolones (27%), tetracyclines (20%), amphenicols (18%), and sulfonamides (14%).

Antimicrobial consumption from humans, terrestrial animals, and aquaculture. Proportion of use across sectors remains relatively consistent through 2030, when human use (48,608 tons), terrestrial food producing animal use (174,549 tons), and aquatic food producing animal use (13,600 tons) represent 20.5, 73.7, and 5.7% of global consumption, respectively.

“Compared with antimicrobial use in terrestrial food animal production, application of antimicrobials in aquaculture provides a potentially wider environmental exposure pathway for drug distribution through water with important ecosystem health implications.”

Discussion Global trends

At current rates, global antimicrobial consumption in aquaculture is expected to increase 33% between 2017 and 2030. These estimates are associated with considerable uncertainty and relatively wide uncertainty intervals due to the scarcity of point prevalence surveys on antimicrobial use in aquaculture. Global trends in antimicrobial use in aquaculture are heavily influenced by the expansion of aquaculture in Asia, and particularly in China.

Collectively, the five countries with the largest projected relative increase in antimicrobial consumption between 2017 and 2030 account for only 11.5% of global antimicrobial consumption in 2030, indicating that, with the exception of Indonesia, the countries with the fastest antimicrobial consumption growth will remain the minority contributors to global consumption projected by 2030.

At a country-level, few estimates of antimicrobial use in aquaculture have been produced. Although this limits comparisons of our estimates with country-level use, our antimicrobial use estimates for aquaculture are within the range of a 2013 domestic consumption estimate from China, and approximately 40% of the low bound from a 2002 estimate in the United States.

Drug classes and species

All of the classes of antimicrobials identified in our systematic review of point prevalence surveys are classified by the World Health Organization as important for human medicine. Classes assigned to the top two classification tiers—highly important and critically important antimicrobials for human medicine—collectively represented 96% of all use (Supplementary Fig. S4).

This finding is of particular concern given that few alternatives to these drug classes exist. It further raises the prospect of antimicrobial use in aquaculture driving resistance trends in aquatic environments, with implications for transfer of resistance genes across bacterial species. Such transfers are ecological in nature and are thus challenging to document.

However, the transmission of resistance genes across bacteria capable of spanning the aquatic–environment–human interface with corollary public health impact, as has been described in terrestrial food producing animal settings, has been suggested.

This dynamic may be particularly important in areas reliant upon untreated water sources and with higher rates of consumption of raw fisheries products.

Several countries have experienced dramatic reductions in antimicrobial use rates following introduction of vaccination and improved management and husbandry programs, serving as important antimicrobial stewardship models.

Limitations

Our antimicrobial consumption projections are subject to wide uncertainty intervals that likely reflect both the limited availability of surveys, from which projections were generated, and the diversity of global aquaculture production systems, practices and species.

The diversity of farmed aquatic animal species greatly exceeds terrestrial food animal producing species. Currently, antimicrobial use is poorly documented even for those species of greatest production significance.

“At current rates, global antimicrobial consumption in aquaculture is expected to increase 33% between 2017 and 2030. These estimates are associated with considerable uncertainty and relatively wide uncertainty intervals due to the scarcity of point prevalence surveys on antimicrobial use in aquaculture.”

Finally, without data capturing temporal trends in species-specific antimicrobial use, we assumed that the mean use coefficients by species remain constant between 2017 and 2030.

As a consequence, variability in anti- microbial consumption solely reflects the growth in aquaculture production in each country or region through 2030. Despite these limitations, our estimates provide a starting point to help frame a discussion outlining nearterm priorities to enhance antimicrobial use data collection.

A confluence of trends in animalsource nutrition availability could push accelerated rates of aquaculture growth in the near-term. Increasing ocean acidification and warming has been projected to represent a net negative impact on capture fisheries output, which have plateaued over the last two decades.

And terrestrial animal epizootics, such as African swine fever in Asia, are constraining terrestrial animal-source nutrition supply. In this context, an acute reorientation of protein demand to aquatic animal-source food products could be expected to drive increased aquaculture production output.

“Several countries have experienced dramatic reductions in antimicrobial use rates following introduction of vaccination and improved management and husbandry programs, serving as important antimicrobial stewardship models.”

Under business as usual conditions, this would lead to an increase in antimicrobial consumption in aquaculture. Such trends could be significant in areas with widespread availability of—and unrestricted access to—antimicrobials.

Robust surveillance data (1) facilitates identification of sectors and production contexts where either inappropriate use or lack of access would benefit from rebalancing; (2) enables the establishment of timebound, measurable consumption targets and monitoring progress toward achieving these targets; and (3) when paired with resistance data, generates additional insight into the association between patterns of consumption and anti- microbial resistance trends.

A tiered approach to surveillance of antimicrobial consumption permits utilization of existing sales channel data to direct enhanced stewardship policies while structures are developed to produce iteratively more granular, farm-level consumption data.

“As a function of potentially higher rates of off-label use of antimicrobials in aquaculture—particularly in developing country contexts—sales data, however, may currently under-represent consumption. Labelled indications for therapeutic use in primary aquaculture species will improve attribution to—and characterization of—aquaculture use.”


Our findings call for urgent strengthening of surveillance for antimicrobial consumption and enhanced understanding of antimicrobial resistance transmission risk across the aquatic animal–environment–human interface, with application of targeted policies and regulatory structures promoting antimicrobial stewardship and antimicrobial efficacy as a shared global resource.

* This is a summarized version developed by the editorial team of Aquaculture Magazine based on the review article titled “Global trends in antimicrobial use in aquaculture” developed by: Daniel Schar, EiliY. Klein, Ramanan Laxminarayan, Marius Gilbert, and Thomas P. Van Boeckel. The original article was published on 2020, through the Scientific Reports Journal of Nature Research under the use of a creative commons open access license. The full version can be accessed freely online through this link: https://doi.org/10.1038/ s41598-020-78849-3

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