1. Introduction
Aquaculture is a growing productive activity worldwide, providing sources of food and economic income for the population of many countries [
1,
2]. One of the most important sectors of aquaculture in Chile is the production of farmed salmon [
3]. With more than 1000 tons of salmon biomass harvested, the country is considered the second largest salmon producer in the world [
4]. However, the sustainability of its national industry has been affected by the high use of antibiotics to control relevant bacterial infections, such as
Piscirickettsia salmonis (Salmon Rickettsial Syndrome or SRS) and
Renibacterium salmoninarum (Bacterial Kidney Disease or BKD) [
5,
6]. Despite the reduction in their use for almost a decade, Chile still shows the highest consumption rates of the use of antimicrobials per ton of salmon produced in the world with approximately 380 tons of antibiotics used in 2020 [
4]. This intense use of antibiotics, especially florfenicol and oxytetracyclines, could result in selecting antibiotic-resistant-bacteria (ARB) and/or antibiotic-resistance genes (ARGs) [
7].
The mitigation of the antimicrobial resistance (AMR) phenomenon has been considered a priority by the World Health Organization (WHO), the Food and Agriculture Organization of the United Nations (FAO), and the World Organization for Animal Health (OIE). These institutions have established a tripartite intersectoral collaboration (
https://www.fao.org/publications/card/en/c/CA2942EN, accessed on 11 May 2022) to address key points to tackle AMR at the human–animal-environment interface, which includes the extensive use of antibiotics in animal production systems [
8]. Chile has also adopted various national regulations to control and reduce the use of antimicrobials. A good example is the implementation of electronic prescriptions for aquatic animals (issued exclusively by veterinarians), allowing real-time surveillance as part of the “National Plan to Combat Antimicrobial Resistance” launched in 2017 by the Ministry of Health [
9]. In addition, multiple sanitary control procedures are established in the “Manual of Good Practices in the Use of Antimicrobials and Antiparasitics in Chilean Salmon Farming” that salmon producers must follow [
10], and there are also initiatives coordinated by non-governmental organizations, such as the “Chilean Salmon Antibiotic Reduction Program (CSARP,
https://www.csarp.cl/, accessed on 11 May 2022)”. However, diseases such as SRS and BKD are difficult to control and have resulted in a massive use of florfenicol and oxytetracycline in farmed salmon [
4,
5], increasing the risks of AMR.
Limited research has been carried out to study the impact of the consumption of antibiotic-treated salmon fillet on public health [
7,
11]. Previous studies have reported that the use of antimicrobials in animals has been positively associated with the likely emergence, maintenance, and spread of ARB and ARGs [
12,
13,
14]. Other studies suggest that food derived from treated animals would more likely harbor ARB and ARGs, posing a risk of transmission to consumers, especially when eating raw (e.g., seafood) or undercooked meats [
7,
15,
16]. Despite this, it remains unclear whether reduction in the use of antibiotics in food animals could directly lower the risk of AMR acquisition by humans (especially those consuming animal-origin food).
Consulting the opinion of professionals with proven expertise in a particular field of interest has been widely used when there are insufficient baseline data for immediate interventions with informed decision making, as well as promoting communication and awareness of the need to study a specific topic [
6,
17,
18,
19]. Through a systematic process of information gathering, evaluation, and documentation, a qualitative or quantitative risk assessment enables the assignment of a level of probability of occurrence for a specific event until more accurate information is available [
7,
20,
21,
22,
23]. The aim of this study was to determine the multisectoral risk perception of AMR through salmon fillet consumption and to provide estimates of risk levels in each step of the salmon production cycle, using a structured expert elicitation process based on validated methodologies [
21,
24]. In addition, this expert elicitation highlighted production issues that could impact the Chilean farmed salmon trade and markets and, consequently, the sustainability of the national industry. This risk assessment could help decision makers in salmon farming systems to identify the most necessary steps for interventions to reduce the amount of antibiotics needed, achieve economic sustainability, and reduce AMR in aquatic animal production.
3. Results
During the expert workshop, a flowchart was collaboratively constructed in which nine nodes (i.e., events) were identified by combining opinions from five independent groups of experts. Each node corresponds to an event that could be related in some way to human acquisition of ARB and/or ARGs from consumption of salmon fillet treated with florfenicol or oxytetracycline (
Table 3).
Nodes were clustered and then classified into three groups: ‘Antibiotic Release’, ‘Exposure’, and ‘Consequence’ (
Figure 1). The events that could have causal or influential relationships are connected by dotted lines, while the direction of sequential events is indicated by arrows. The lack of connectors represents conditional independence since the probability of a specific node may (or may not) be affected by previous ones. For example, the occurrence of one or more nodes within ‘Antibiotic Release’ could increase the probability of nodes within the ‘Exposure’ group, although these could also occur independently of nodes 1, 2, or 3.
The results of the expert elicitation obtained through the discussions during the workshop, including the identification of the nodes, and from the questionnaires answered by each expert individually, were used to generate a diagram of the salmon production within the farm settings (i.e., freshwater phase, seawater phase, and processing chain) (
Figure 2).
A total of 34 scenarios were identified throughout salmon farming, including 11 from the freshwater phase (
Figure 2A), 14 from seawater (
Figure 2B), and 9 from the processing chain (
Figure 2C). A brief description of the scenarios analyzed, corresponding to steps or situations within the salmon production, is provided in
Table 4.
In the created diagram (
Figure 2), scenarios were represented by rectangles, and those that were considered to have a causal or influential relationship with each other were connected by solid lines. It was possible to obtain the multisectoral risk perception of 38 pathways among scenarios by eliciting expert data. These (uni- or bidirectional) routes of transmission within the salmon production are indicated in the diagram by arrows, including 12 in the freshwater phase (
Figure 2A), 15 in the seawater phase (
Figure 2B), and 11 in the processing chain (
Figure 2C).
Overall, there was a consensus between academia, public sector, and salmon industry experts that the risk of acquiring ARB and ARGs from consumption of treated salmon might be ‘low’, and most pathways identified as threats during the production of farmed salmon were ranked with a risk level between ‘insignificant’ and ‘low’ (nodes might occur under exceptional circumstances or sporadically, respectively). However, experts broadly agreed that risks were most likely associated with bacterial infections and antibiotic therapies. The risk analysis showed a perception that the freshwater phase of salmon production would have a proportionally larger number of pathways associated with at least a ‘low’ level of risk (67%, 8/12,
Figure 2A) compared to the seawater phase (60%, 9/15,
Figure 2B) and the processing chain (36%, 4/11,
Figure 2C).
Most pathways with an associated risk in the freshwater production were preceded by the ‘Antimicrobial treatments’ scenario towards the ‘Broodstock’, ‘Eggs’, and ‘Fry’ scenarios (
Figure 2A). The pathway between the scenarios ‘Antimicrobial treatments’ and ‘Eggs’ had the highest level of risk assigned (‘moderate’) as ‘Eggs’ is one of the scenarios in which most treatments are carried out. In addition, a ‘cyclical risk’ of maintenance of ARB, ARGs, or antibiotic residues among the scenarios ‘Eggs’, ‘Fry’, and ‘Smolts’ was identified by the experts due to the possibility of water reuse and/or poor cage cleaning. Bacterial diseases were also included in the flowchart, not only because of their causal relationship to the need for antibiotic therapies, but also because they result in a risk of ARB/ARG emergence from the increased use of antibacterial products needed for disinfection. A ‘low’ risk was also perceived in releasing waste in the water sources used in this phase due to the possibility of absence of water treatment before use by salmon farms.
Like the freshwater phase, many risk pathways in the seawater phase of the salmon production were related to antimicrobial usage. ‘Grow fat’ was the scenario with the highest number of perceived risk pathways, both toward the earlier and later scenarios (
Figure 2B). The staff were also perceived to pose a risk for the emergence and spread of ARB and ARGs that was mainly associated with the handling of farmed salmon infected with bacterial diseases and the administration of antibiotics to these animals. Additionally, a perception of low risk was linked by some experts to AMR pollution from anthropogenic sources (i.e., wellboats, boats, and trucks) and to the influential relationship within the environment (between wild animals and escaped salmon). However, when gathering all qualitative estimations and converting to our ordinal-scale ranking (from 0 to 3), the risk in the pathways associated with both scenarios was quantified as less than 1, and it was considered as ‘insignificant’.
Concerning the processing chain, in all internal pathways some degree of risk was identified (
Figure 2C). Nonetheless, the risk of the pathway after the ‘Evisceration and removal of bones and head’ scenario was rated as ‘insignificant’ (less than 1 on our ordinal scale) and the remaining ones were considered as ‘low’. On the other hand, as opposed to the results obtained for the seawater phase, no external factors (i.e., environmental sources) nor anthropogenic contamination were associated with an AMR risk.
4. Discussion
The high use of florfenicol and oxytetracycline during salmon farming to control bacterial diseases (e.g., SRS and BKD) could represent a public health concern. However, it is unclear whether the consumption of farmed salmon treated with antibiotics may be a determining factor for the acquisition of ARB and/or ARGs by the human population. In the absence of scientific evidence, this risk was explored by 24 experts of different areas that evaluated the main scenarios and pathways within salmon production as a first approach to generate baseline knowledge and encourage studies in the field. There was a perception of ‘low’ risk of ARB and ARGs among the population through salmon consumption. However, most of the pathways assigned with some degree of risk were those preceded by the use of antimicrobials, highlighting that the control of bacterial diseases requires special attention.
The presence of professionals from academia, the public sector, and the salmon industry sectors provided a comprehensive and holistic understanding of the risks of AMR from the consumption of salmon fillet. As this is a multidisciplinary problem, professionals from the salmon industry were included to capture the perception within the national salmon farming routine. Importantly, none of the salmon industry participants were farmers or directly involved in salmon production, but service providers for the salmon farms (i.e., scientific, technical, and/or diagnostic support). All experts had a proven scientific background and formed a well-balanced panel of experts, which allowed for the inclusion of different perspectives, as recommended by other authors [
21].
A higher proportion of risk pathways (perceived as ‘low’ or ‘moderate’ risk) was identified in the freshwater phase (
Figure 2A). However, most diagnostics and preventive measures are mainly carried out in the seawater phase, probably because of the low economic impact bacterial diseases have in the freshwater phase [
31,
32,
33]. The use of antibiotics in the freshwater phase is common and may represent an important risk factor for the emergence of AMR [
7,
12,
13,
34,
35]. In fact, ‘Eggs’ was the scenario with the highest assigned risk (‘moderate’) (
Figure 2A) due to the high frequency of individual antibiotic treatments on all animals in the cage. Another concern is about the available data from the freshwater phase. While electronic prescriptions are a good source of information on amounts of antibiotics used in this phase, other relevant data are not adequately recorded (e.g., frequency of detection of bacterial AMR infections, number of unresponsive antibiotic treatments) [
32,
33]. Insufficient efforts to diagnose and prevent bacterial disease, high frequency of antibiotic use, and limited data recording demonstrate that the freshwater phase should be a priority for intervention to improve data recording and to implement initiatives seeking to reduce antibiotic use.
Risks were clearly associated with bacterial infections and the consequent use of oxytetracycline and florfenicol. Good sanitary practices are essential for reducing infectious diseases [
36,
37]. However, strategies should go beyond the use of antibacterial products that also contribute to the selection of resistant pathogens [
38,
39]. Promoting proper disposal of organic matter, hand washing when handling sick animals, ensuring good animal nutrition, reducing animal stress, and avoiding overcrowding could help prevent and control bacterial infections. The reduction in antibiotic treatments could also be reflected in less aquatic environmental contamination, thus decreasing public health risks. It is estimated that 75% of antibiotics fed to fish are not metabolized, exacerbating this contamination if waters are not treated before being returned to rivers [
7]. In addition, antibiotic administration in salmon farming is mainly carried out through medicated feeds, which have lower palatability and may favor the spread of antimicrobial residues through degraded feed [
5,
33,
40,
41,
42,
43,
44]. To our knowledge, there is no surveillance or monitoring of the water sources used on salmon farms, which could be affecting other food production systems intended for human consumption that are supplied by the same rivers, such as livestock and agriculture irrigation.
To our knowledge, this is the first study in Latin America to review the entire salmon production chain and the potential human health risks associated with the emergence and spread of ARB and ARGs through the consumption of farmed salmon. Despite the intense use of antibiotics during the salmon production in Chile, the risk of occurrence and spread of ARB and ARGs associated with salmon consumption was understood as ‘low’. National initiatives, such as the prohibition of prophylactic treatments, mandatory diagnosis before treating a bacterial disease, and the surveillance program for oxytetracycline and florfenicol resistance in
P. salmonis (SRS) [
9,
10,
33,
45], could be some reasons for experts to consider the risk of AMR by salmon consumption to be low. The data obtained up to 2020 have shown no resistant isolates of
P. salmonis to oxytetracycline or florfenicol. However, 90% of the isolates obtained in 2019 presented a reduced susceptibility to florfenicol and 70% to oxytetracycline [
33,
46]. This corroborates the experts’ conclusions, since it shows that the risk exists but, as it is a slow phenomenon, the risk is therefore very low. The implementation of the antimicrobial surveillance program for
R. salmoninarum (BKD) and
Flavobacterium psychrophilum in 2020 should provide more information on the trends of the AMR phenomenon in the main bacterial pathogens of farmed salmon in Chile.
Although there is evidence that this low risk is realistic and representative of the current situation, the possibility of underestimation cannot be ruled out. Moreover, the experts contributed their knowledge according to their field, and the estimates were not weighted. Therefore, the questionnaires do not have the same response rate, and a possible survey response bias could not be quantified. While rapid risk assessment is useful in identifying the phases and pathways requiring special attention, it can only be considered as preliminary in the comprehensive risk assessment. One way to complement this type of analysis and obtain a more reliable result is to use a One Health approach integrating surveillance focused on organisms that may pose a threat to human health or have the potential to acquire ARGs and develop antibiotic resistance (e.g.,
E. coli) [
7]. Integrated surveillance, which consists of simultaneously investigating AMR in livestock, humans (i.e., patients), and the food production chain using systematized methodology [
47,
48,
49], could help us to quickly assess the consequences to human health arising from different sources. Given its multifactorial characteristics, One Health AMR surveillance could enable early detection of emerging resistance threats and ensure comprehensive data capture for implementation of specific mitigation strategies and AMR risk trends assessment for consumers. Finally, the results of this study yielded the identification of critical points in the salmon production system and areas where research and data collection are necessary to reduce the uncertainty of risk estimates identified in this study. Thus, the same methodology could be used to evaluate other animal production systems that also show high rates of antibiotic use and could represent a public health risk.
5. Conclusions
To the best of our knowledge, this qualitative risk assessment is the first overview of potential risks of AMR for humans from the consumption of salmon fillet by consulting experts from different fields related to public and animal health. Although the possibility of underestimation cannot be excluded, there was a consensus among these sectors on the low, but existing, risk of AMR through salmon consumption. It should also be noted that a possible survey response bias could not be quantified and that this estimate should be considered as preliminary in the comprehensive risk assessment. In addition, this risk was mainly linked to the use of oxytetracycline and florfenicol, particularly in the freshwater phase. Improved data recording and implementation of enhanced preventive measures to mitigate bacterial diseases and reduce antibiotic use at this phase could promote economic sustainability and food safety in relation to AMR from antibiotic-treated salmon consumption. Furthermore, such initiatives could be facilitated by the observed intersectoral alignment. The expert elicitation exposed in this study generates a baseline information of the AMR risks resulting from the consumption of salmon treated with antibiotics and highlights the need for further studies, especially in the steps identified by the experts as priorities. Finally, the present study could be replicated in other countries and/or for other animal productions looking for strategies to curb AMR, especially in scenarios where high amounts of antibiotics are used. A comprehensive strategy using the “One Health” approach is needed to mitigate potential antibiotic resistance in animal production by considering key factors, such as bacterial disease prevalence, antibiotic use patterns, and human–animal interactions.
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