Addressing Antibiotic Use in Aquaculture
Aquaculture, or the farming of aquatic organisms such as fish, crustaceans, mollusks, and aquatic plants, has become an essential part of the global food supply. Globally, aquatic animals provide 17% of animal protein consumed, with fish contributing nearly 20% of per capita animal protein for over 40% of the world's population [1]. As the industry expands to meet the increasing demand for seafood, the use of antibiotics has become a critical tool in maintaining the health of farmed aquatic species. However, this practice raises concerns about the sustainability and safety of aquaculture products.
The Rise of Antibiotics in Aquaculture
The rise in antimicrobial use in both humans and animals is driving antimicrobial resistance, a major global health challenge. This increases the incidence of resistant pathogens in animal production, leading to higher treatment failure rates and undermining sustainable food production and animal welfare [1].
In aquaculture, production intensification and pathogen outbreaks are similarly driving antimicrobial use and resistance across various farmed species. Compared to terrestrial animal production, aquaculture presents broader environmental exposure to antimicrobials through water, affecting ecosystem health. Antimicrobial residues in water alter the environmental microbiome, impacting nutrient cycling, biodiversity, carbon sequestration, and freshwater availability [1].
Moreover, aquaculture settings that use antimicrobials can serve as reservoirs for antimicrobial resistance genes, facilitating human and animal exposure to resistant bacteria. Shared resistance genes among pathogens from humans, terrestrial and aquatic animals, and the environment indicate pathways for resistance gene transfer. For instance, the emergence and spread of plasmid-mediated colistin resistance genes are believed to originate from aquaculture [1].
Uses of Antibiotics in Aquaculture
Prophylactic Use
Prophylactic use involves administering antibiotics to all animals in a population before any signs of disease to prevent the onset of bacterial infections. Antibiotics are given at sub-therapeutic levels to minimize the risk of disease outbreaks, particularly in high-density farming environments where the spread of pathogens can be rapid and devastating [2].
Therapeutic Use
Therapeutic use refers to the administration of antibiotics to treat animals that are already showing symptoms of bacterial infections. This targeted approach involves identifying the specific infection and administering the appropriate antibiotic to affected animals to reduce mortality and morbidity rates [2].
Metaphylactic Use
Metaphylactic use involves mass medication of a group of animals when an outbreak is expected or when some animals within the group are already showing symptoms of disease. This strategy is employed to control and limit the spread of the disease, treating both sick and healthy animals to ensure that the infection does not escalate [2].
Growth Promotion
Growth-promoting antibiotics are administered to animals to enhance their growth rates and improve feed efficiency. By altering gut microbiota and improving nutrient absorption, these antibiotics help animals grow faster and convert feed into body mass more efficiently. Although this practice is becoming less common due to rising concerns about antibiotic resistance, it has historically been used to maximize production efficiency in aquaculture operations [2].
Risks Associated with Antibiotic Use
Each of these the above uses of antibiotics has specific applications and benefits, but they also come with significant risks, particularly concerning the development of antibiotic-resistant bacteria. Prophylactic and metaphylactic uses, in particular, can contribute to the spread of resistance due to the widespread exposure of bacteria to sub-therapeutic levels of antibiotics. As a result, the industry is increasingly under scrutiny to find alternative methods and practices to ensure the health and productivity of aquaculture systems without relying heavily on antibiotics.
Antibiotic Resistance
One of the most significant risks associated with antibiotic use in aquaculture is the development of antibiotic-resistant bacteria. These resistant bacteria can spread to wild populations, other animals, and humans, posing a severe public health threat. Even at concentrations below the minimum inhibitory concentration (MIC), antibiotic residues can select for resistant aquatic bacteria, promoting the spread of antibiotic resistance [2].
High frequencies of antibiotic-resistant bacteria have been reported near aquaculture sites where antibiotics are used. This demonstrates that antibiotics in aquaculture facilities can exert selective pressure, increasing the prevalence of antibiotic resistance in other environmental bacteria. Studies indicate that 90% of aquatic bacteria in these environments are resistant to at least one antibiotic, and about 20% are multi-resistant. The simultaneous use of different antibiotics in aquaculture can lead to the development of multi-resistant bacteria. Additionally, bacteria with novel resistance mechanisms have been detected in these settings [2].
The survival advantage conferred by antibiotic resistance allows resistant bacteria to thrive over susceptible ones, leading to a higher prevalence of resistant strains in the environment. A particularly concerning aspect is that many antibiotics used in aquaculture are also used in human medicine, potentially inducing resistance to these human drugs as well [2].
Transfer of Antibiotic Resistance to Humans
Aquaculture sites are considered hotspots for antibiotic-resistant genes. Bacteria harboring these genes can proliferate and spread according to environmental conditions, disseminating resistance across various locations. The aquatic environment often contains human and animal bacterial pathogens, facilitating the exchange of genetic material between aquatic and terrestrial bacteria [2].
Horizontal gene transfer (HGT) plays a crucial role in the spread of antibiotic resistance genes. The set of mobile genetic elements, known as the mobilome, can move among aquatic bacteria to transfer resistant genes. Aquatic environments with aquaculture facilities create unique conditions that promote HGT. Biofilms on organic particulate matter, sediments, and fish farm structures, combined with high concentrations of bacteriophages and gene transfer agents in seawater, enhance the transfer and spread of antibiotic resistance [2].
This genetic material can be transferred to human pathogens, such as Vibrio cholerae, Vibrio parahaemolyticus, Vibrio vulnificus, Shigella spp., and Salmonella spp.. Transmission to humans can occur through direct contact with water or aquatic organisms, consumption of seafood, or handling practices. Antimicrobial resistance in bacteria causing human infections leads to several serious consequences including more frequent infections, higher rates of treatment failure, increased severity of illnesses, higher hospitalization rates, and mortality [3].
Environmental Impact
Antibiotics can accumulate in the aquatic environment, affecting non-target organisms and disrupting ecosystems. These substances are often not fully metabolized by fish and are released into the water, where they contribute to the spread of antibiotic-resistant microbes and impact ocean health. Antibiotic administration in aquaculture often involves mixing antibiotics with feed, leading antibiotics to accumulate in the aquaculture environment [4].
Effluents from aquaculture farms containing antibiotic residues are often discharged into rivers or used as manure on farmlands, leading to further environmental contamination. These residual antibiotics can enter the food chain, causing various ecological disruptions. They can affect phytoplankton and zooplankton diversity, disrupt zooplankton developmental processes, and inhibit phytoplankton chlorophyll production. Such disruptions can alter the food chain, impacting the entire ecosystem [4].
Antibiotic Residues in Seafood
Antibiotic residues are trace amounts of these drugs or their metabolites found in edible portions of aquatic animals after administration. The presence of antibiotic residues in cultured aquatic products can be systemically toxic to consumers and negatively impact the human gastrointestinal microflora. Chloramphenicol residues, for example, increase the risk of cancer and, even at lower concentrations, can cause aplastic anemia. Other health issues related to residual antibiotics include penicillin hypersensitivity, gentamicin-induced mutagenicity and nephropathy, and the immunopathological and carcinogenic effects of sulfamethazine, oxytetracycline, and furazolidone [4].
Alternatives to Antibiotic Use
Vaccines
Vaccines play a critical role in reducing antibiotic use by preventing infectious diseases in fish. Developed from pathogenic microorganisms or their derivatives, vaccines are modified to effectively stimulate immune responses and prevent diseases. They have become indispensable tools in disease prevention strategies, exemplified by their use in Norwegian salmon farming, where their implementation led to a substantial decrease in antibiotic usage [5].
In the 1980s and early 1990s, the Norwegian salmon industry faced severe bacterial infections and the emergence of infectious salmon anaemia (ISA), prompting the establishment of a national biosecurity program involving government, industry, and research institutions. By the early 1990s, this program, supported by the development and widespread adoption of effective vaccines, notably against furunculosis and cold-water vibriosis, significantly reduced antibiotic use in salmon farming. Annual antibiotic consumption dropped from nearly 50 metric tonnes in the early 1990s to between 500 kg and 1500 kg since 1996. Today, Norway routinely vaccinates juvenile Atlantic salmon before sea transfer, employing various vaccines tailored to specific pathogens. Despite the lifting of mandatory vaccination requirements in 2009/2010, the industry continues to vaccinate voluntarily, contributing to its sustained growth and dominant position in global salmon production and seafood export [5].
Bacteriophages
Bacteriophages, also known as phages, are viruses that infect bacterial cells, causing them to disrupt and lyse. Discovered in the early 1900s, phages initially showed promise in controlling bacterial diseases before antibiotics took precedence. Now, with increasing antibiotic resistance, phage therapy is gaining renewed attention. Phages are abundant globally, especially in marine and freshwater environments, where they can survive for extended periods. Their survival is generally unaffected by pH, salinity, temperature, or organic matter concentration, though specific conditions may influence certain phage types. Phages can exist in bacterial DNA as prophages or as replicons, with variable impacts on bacterial virulence and genetic traits. In aquaculture, phage therapy has been effective against bacterial pathogens like Vibrio species, though challenges remain in developing broad application. Research continues into phage-host interactions, genetic diversity, and co-evolution dynamics, essential for advancing phage-based therapies in aquaculture and beyond [5].
Quorum Quenching
Quorum quenching (QQ) refers to disrupting quorum sensing (QS), a bacterial mechanism that regulates gene expression based on population density. QS enables bacteria to coordinate various behaviors crucial for pathogenicity and survival, such as biofilm formation and toxin production, through the release and detection of small signaling molecules [5].
By disrupting QS signals through QQ methods—such as enzymatic degradation of signaling molecules or competitive inhibition—researchers aim to attenuate bacterial virulence and inhibit biofilm formation. This approach not only directly mitigates bacterial pathogenicity but also indirectly reduces the need for antibiotics [5].
Probiotics
Probiotics, consisting of live microorganisms like Lactobacillus and Bifidobacterium, are widely used to enhance gut microbial balance and are administered as dietary supplements. They inhibit harmful bacteria through various mechanisms, such as competing for nutrients and producing antimicrobial compounds like bacteriocins. Probiotics also synthesize essential nutrients like polyunsaturated fatty acids and vitamins, and some strains help in organic pollutant assimilation, thereby improving the rearing environment [5].
Prebiotics, non-digestible carbohydrates like oligosaccharides, selectively stimulate beneficial gut bacteria fermentation, thereby promoting a healthy microbiome. Combining probiotics and prebiotics into synbiotics enhances their beneficial effects, supporting host immunity and overall health. Parabiotics, consisting of dead probiotic cells, and postbiotics, metabolic by-products from probiotic cultures, also influence microbiome health and disease occurrence [5].
Advanced metagenomic techniques like next-generation sequencing have revolutionized microbiome research by identifying previously undetected bacterial species. These discoveries provide insights into microbiome dynamics and offer potential alternatives to antibiotics, aiming to stabilize and enhance the health of aquatic organisms through microbiome management [5].
Managing the Use of Antibiotics
Regulation
Regulating the use of antibiotics in food animals is crucial to combat antimicrobial resistance. The World Health Organization (WHO) has advised national veterinary, agricultural, and pharmaceutical authorities, along with other stakeholders, to phase out the use of antibiotics as growth promoters. They advocate for antibiotics to be administered to animals strictly under veterinary supervision and recommend reserving critically important antibiotics for human medicine [6].
Responsible Use of Antibiotics in Aquaculture
Antibiotics are crucial medications that should be employed sparingly and solely for therapeutic purposes. National veterinary, agricultural, and pharmaceutical authorities play a pivotal role in advocating for preventive veterinary care and the judicious use of antibiotics. Collaboration with private sectors, including veterinary practitioners and farmers, is essential in ensuring responsible antibiotic management [6].
First, reducing the need for antibiotics should be prioritized by enhancing animal health through rigorous bio-security measures to prevent the introduction and spread of harmful bacteria. Additionally, disease prevention strategies such as effective vaccines, prebiotics, and probiotics play a crucial role. Good hygiene and management practices further contribute to minimizing the necessity for antibiotics [6].
Furthermore, antibiotics should only be administered to food animals under the direct prescription of a veterinarian. Their usage should strictly adhere to therapeutic purposes, guided by resistance surveillance results from microbial cultures and antibiotic susceptibility tests, as well as clinical judgment. The practice of using antibiotics as growth promoters should be completely phased out to curb unnecessary antibiotic use [6].
In cases where antibiotic therapy is necessary, preference should be given to narrow-spectrum antibiotics whenever feasible. Critically important antibiotics used in human medicine, notably fluoroquinolones and third- and fourth-generation cephalosporins, should be reserved for animals only when clearly justified [6].
Surveillance
Monitoring antibiotic resistance in zoonotic and commensal bacteria across various food animal reservoirs and aquaculture products is crucial for comprehending how resistance evolves and spreads. This surveillance is essential for conducting risk assessments and implementing targeted interventions effectively. It involves ongoing data collection, thorough analysis, and continuous reporting to track temporal trends in antibiotic resistance distribution. To ensure prompt corrective actions and evaluate interventions, public health, veterinary, and food authorities are advised to establish surveillance systems for antibiotic usage in both human and animal sectors. Additionally, integrating surveillance across public health, food, and veterinary domains can effectively monitor antibiotic resistance in selected foodborne bacteria [6].
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