Bacterial Resistance in the Finfish AFquaculture and Alternatives: Comparison
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Significant challenges to worldwide sustainable food production continue to arise from environmental change and consistent population growth. In order to meet increasing demand, fish production industries are encouraged to maintain high growth densities and to rely on antibiotic intervention throughout all stages of development. The inappropriate administering of antibiotics over time introduces selective pressure, allowing the survival of resistant bacterial strains through adaptive pathways involving transferable nucleotide sequences (i.e., plasmids). This is one of the essential mechanisms of antibiotic resistance development in food production systems.The AMR phenomenon has been generally defined as the failure of growth’s inhibition or the killing capacity of an antimicrobial molecule beyond the normal susceptible bacteria.

  • aquaculture
  • finfish
  • antibiotic molecule

1. Introduction

Comparing aquaculture to the terrestrial farms, based on pharmacological consumption, researchers have highlighted significant differences. Indeed, the World Health Organization classified aquaculture as an activity with a low environmental impact for antibiotic usage [1][2]. Directly linked to the above-explained concepts, veterinarians play key roles in pharmacological management. This consideration is justified because this professional figure firstly prescribes antibiotic therapies, avoiding the unnecessary administering (as metaphylactic one) of certain classes—in which usage is restricted to the human medicine: the so-called Critical Importance Antimicrobials WHO (CIA)—for food-producing animals; secondly, they must reduce administering to only restricted specific cases. The aim is to decrease a relevant selective pressure, which promotes resistant and pan-resistant bacterial strains survival [3]. These strains are named as antibiotic resistance bacteria (ARBs) that can be considered as “drivers” of antibiotic resistance genes (ARGs) with important repercussions on the environmental, animal, and human health [4]. It has been widely demonstrated that ARGs can be transferred to human intestinal microbiota and, consequently, to the ingestion of foods (numerous matrices: meat, dairy products, fish, etc.), which can drive commensal or pathogenic (Salmonella spp., Vibrio spp.) ARBs with extra chromosomal resistance forms. Finally, it is important to mention possible drugs residues due to the improper observation of legal limits [1]. Therefore, the European Regulations No. 470/2009 and No. 37/2010 established the residual limits of pharmacologically active substances in animal origin foodstuffs.

2. Antibiotic Resistance Bacteria Isolation and Antibiotic Resistance Genes Detection from Aquaculture Finfish Samples

The finfish aquaculture zootechnic sector has been characterized by a wide range of farming techniques as the embankment ponds or the watershed ones (as observed in the catfish (Clarias spp., Ictalurus spp., and Pangasius spp.) culture) [5], mariculture systems (i.e., for Salmo spp., Sparus spp., [6], intensive or semi-intensive inland pond systems for Tilapia spp. [5]), and other animals finfish species, etc.
In the above-mentioned systems the high animal densities have induced the necessity of antibiotic administering for therapeutic purposes. This last-explained concept was associated with possible inappropriate usages and has selected resistant pathogens or commensal bacterial strains. More in detail, tetracyclines, beta-lactams, quinolones, and sulfonamides antibiotic classes have been largely prescribed by veterinarians. Therefore, biomolecular diagnostic procedures have coupled the next generation sequencing to the bacterial whole genome analysis. This last cited method has permitted reusearchers to discover new oligonucleotide resistance determinants [7]. Oligonucleotide sequences are the main actors involved in the ARGs circulation and are, consequently, responsible for the presence of vector bacteria (not usually resulting in pathogens for humans) while constituting crucial environmental reservoirs for the human and animal host microbiota [8]. For these reasons, animal origin foodstuffs have acquired more attention from scientists. The reasons were firstly related to possible residual concentration, but more specifically the main concern is represented by the possibility of horizontal resistance genes transmission between alimentary commensal and opportunistic strains with the human microbiota. Indeed, microorganisms have elaborated numerous mechanisms to disseminate the ability to survive by mobile genetic elements, such as integrons, plasmids, insertion sequences, transposons, and gene cassettes [8][9], and the inappropriate antibiotic usage has produced a selective pressure and the consequential survival of resistant microorganisms (engendering multiple resistances).
Every year, bacterial genome sequencing allows the identification of emerging and re-emerging ARGs, and the most frequent examples are amplified from aquaculture seafood products, i.e., sul (sulfonamides resistance genes), tet (tetracyclines resistance genes), aa (aminoglycosides resistance genes), and bla (β-lactams resistance genes) [10][11][12][13]. Indeed, molecular biology, through the sequencing assays, constantly discovers different mutations among ARGs. There are numerous cases in which there is no matching between discovered phenotypic resistances results with the genotypic ones. This sentence offers explanations based on the concept of nucleotide sequences’ mutations that produce different DNA transcriptions (improper enzymes’ actions), or it is possibly correlated to an intrinsic resistance, which is typical of certain bacterial families against specific antibiotic molecules or classes. The scientific community, during these years, has investigated the AMR diffusion in various finfish species, especially in aquaculture systems, and the respective numerous genera of pathogenic and opportunistic bacteria that are generally implicated in seafood-borne diseases are Vibrio spp. (i.e., V. parahaemolyticus, V, vulnificus), Listeria monocytogenes, Clostridium botulinum, Aeromonas spp., Salmonella spp., Escherichia coli, Campylobacter jejuni, Shigella spp., Yersinia eneterocolitica, Bacillus cereus [14], Pseudomonas spp. [15], and Enterococcus faecium [16] (see Table 1). As previously mentioned, quinolones, tetracyclines, amphenicol, and sulfonamides are major antimicrobial classes used in aquaculture on a global scale [15].
Table 1. AMR* and MDR* of bacterial strains isolated from aquaculture finfish sample tissues.
Country Finfish Samples

n.		 Isolated Bacterial Strains Phenotypic AMR*/MDR* References
Brazil n. 101

Oreochromis niloticus		 Salmonella spp.

(46 isolates)		 Amoxicillin/Clavulanic acid (87.7%)

Tetracycline (82.5%)

Sulfonamide (57.9%)

Chloramphenicol (26.3%)

56:1% of Salmonella spp. isolates were MDR:

Beta-lactam (blaCTX gene 66.7%)

Tetracycline (tetA gene 54.4%)

Chloramphenicol (floR gene 50.9%)

Sulfonamide (sul2 gene 49.1%)		 [17]
n. 50

Cyprinus carpio

n. 50

Oreochromis niloticus		 Enterococcus faecalis

(79 isolates)		 Tetracycline (57.7% tetL and tetM)

Erythromycin (31.01% msrC)		 [18]
China n. 50 fish samples:

Aristichthys nobilis

Carassius auratus

Ctenopharyngodon idellus

Parabramis pekinensis		 Vibrio cholerae

(370 isolates)		 MDR:

Streptomycin (62.2%) 230

Ampicillin (60.3%) 223

Rifampicin (53.8%) 199		 [19]
n. 17

Acipenser spp.		 Streptococcus iniae

(18 isolates)		 Tetracycline (35.6% tetA-02)

Beta-lactams (25.3% blaTEM)

Aminoglycosides (22.1% aadA1)		 [20]
n. 75

Carassius auratus		 Aeromonas hydrophila

(n. 28 isolates)		 MDR:

Penicillin (100%)

Ampicillin (100%)

Amoxicillin (96.4%)

Piperacillin (92.9%)

Cefalexin (78.6%)

Doxitard (75%)

Teicoplanin (67.9%)		 [21]
India n. 25

Oreochromis niloticus		 Pseudomonas entomophila

Aeromonas hydrophila		 MDR:

Bacitracin (100%)

Ampicillin (70%)

Cephalothin (60%)

Cafazolin (50%)

All resistant to:

Amoxicillin

Ampicillin		 [22]
n. 97

Mugil cephalus		 Listeria monocytogenes

(n. 21 isolates)		 69% of Listeria isolates were MDR to:

Ampicillin

Penicillin

Erythromycin

Tetracycline

Clindamycin		 [23]
Armenia n. 25

Oncorhyncus mykiss		 Pseudomonas spp.:

P. anguilliseptica

P. fluorescens

P. stutzeri

P.putida

P. aeruginosa

P. algaligenes		 Resistance percentages:

Piperacillin (45.6%)

Pefloxacin (33.3%)

Ciprofloxacin (3.2%)

All susceptible to:

Chloramphenicol		 [15]
Italy n. 300 fish samples:

n. 100 Dicentrarchus labrax

n. 100 Umbrina cirrose

n. 100 Sparus aurata		 Vibrio spp.

Aeromonas spp.

Shewanella spp.

Photobacterium spp.		 Resistance percentages:

Tetracycline (11.54%) (147/1274)

Trimethoprim/Sulfadiazine (7%) (89/1274)		 [24]
Vietnam n. 50

Ictalurus spp.		 Pseudomonas spp.

(n. 116 isolates)		 Ampicillin (99.1%)

Sulfamethoxazole (93.1%)

Chloramphenicol (88.8%)

Nitrofurantoin (90.5%)

Nalidixic acid (90.5%)

Norfloxacin (9.5%)

Ciprofloxacin (8.6%)

Tetracycline (30.2%)

Doxycycline (25%)		 [25]
Aeromonas spp.

(n. 92 isolates)		 Ampicillin (93.5%)

Sulfamethoxazole (60.9%

Chloramphenicol (31.5%)

Nitrofurantoin (25%)

Nalidixic acid (52.2%)

Ciprofloxacin (7.6%)

Norfloxacin (4.4%)
Vietnam

Scotland

Denmark

Norway

France

Bangladesh

Thailand

Indonesia

Ecuador		 n. 44 fish samples:

n. 12 Pangasiodon hypophthalmus

11 Salmo salar

10 Crassostrea gigas

11 Penaeus mongodon		 Escherichia coli (n. 60)

Enterococcus spp. (n.69)

Pseudomonas spp. (n. 26)

Staphylococcus aureus (n. 9)

(246 isolates)		 MDR strains:

n. 7 E. coli

resistant to:

Chloramphenicol

Ciprofloxacin

Ampicillin

Nalidixic acid

Sulfamethoxazole

Trimethoprim

n. 3 Enterococcus faecalis

resistant to:

Chloramphenicol

Gentamicine

Tetracycline

n. 4 Staphylococcus aureus

resistant to:

Chloramphenicol

Kanamycin

Tetracycline		 [26]
Côte d’Ivoire n. 480

Oreochromis niloticus		 n. 1696 strains:

Escherichia coli (15.9%)

Pseudomonas aeruginosa (10.4%)

Bacillus cereus (14.9%)

Enterococcus faecalis (14.2%)

Citrobacter freundii (13.5%)		 Resistance percentages:

Amoxicillin/Clavulanic Acid (5.8%)

Piperacillin and Penicillin (8.7%)

Gentamycin (7.2%)		 [27]
Iran n. 240

Trota iridea		 n. 86

Listeria spp. isolates		 Tetracycline (62.79%)

Enrofloxacin (56.97%)

Ciprofloxacin (38.37%)

Penicillin (36.04%)

Ampicillin (34.88%)		 [28]
*AMR: Antimicrobial resistance. *MDR: Multidrug resistance.

2.1. Quinolones

Quinolone resistances are characterized by the involvement of DNA gyrase and topoisomerase IV, which are bacterial enzymes and quinolones target proteins. These two enzymes are encoded, respectively, by the gyrA and gyrB genes for DNA gyrase, and by the parC and parE genes for topoisomerase IV [29]. Chromosomal mutations in topoisomerases genes decrease drug accumulation and possible resistance driven by mobile elements, such as plasmid-mediated quinolone resistance (PMQR) (Qnr proteins, aac(6)-lb-cr aminoglycoside acetyltransferases and QepA and OqxAB efflux pumps), causing the constitutive or the acquired resistance to these antibiotic molecules. Increased mutations in DNA gyrase and topoisomerase IV, and in quinolone-resistant fish pathogens (Yersinia ruckeri, Flavobacterium psychrophilum, and V. anguillarum), are linked to the extensive administering of these antimicrobic classes worldwide [30][31][32]. Their wide usage was justified to reduce the hatching losses caused by Vibrio spp. infectious outbreaks. The wide detections of modified plasmids have been discovered from aquaculture finfish fillets [33]. The detected bacterial pathogens were A. hydrophila, V. anguillarum, and V. parahaemolyticus, which showed mutations in the quinolone resistance codifying sequences in specific gene regions belonging to gyrA and/or parC [34][35].
Quinolone resistance genes included in the so-called PMQR are: six qnr genes (qnrA, qnrB, qnrC, qnrD, qnrS, and qnrVC) encoding gyrase-protection repetitive peptides; oqxAB, qepA, and qaqBIII encoding efflux pumps; and aac(60)-Ib-cr encoding an aminoglycoside and quinolone inactivating acetyl-transferase [36]. The majority of PMQRs detection was largely amplified from finfish products worldwide; in China Yan et al. [37] found qepA and aac-(6′)-Ib genes as dominant among PMQR genes in aquatic environments and the possibility of co-emergence of resistance to β-lactams; Jiang and coworkers [38] detected qnrB, qnrS, and qnrD, with aac(6′)-Ib-cr in gut samples of farmed fish. Dobiasova et al. [39] found qnrS2, aac(6)-Ib-cr or qnrB17 genes in Aeromonas spp. isolated from tropical freshwater ornamental fish and coldwater ornamental (koi) carps. In Egypt, scientists reported the occurrence of qnr and aac(6)-Ib-cr resistance from fish farm water sample [3].
From an environmental perspective, there is a strict correlation between remarkable anthropic activities as polluted water areas and quinolones ARGs diffusion [40]. Indeed, in Asia (especially in China), fish farmers normally use biofertilizers to improve production [41]. There is a real possibility that these organic molecules are vectors of antibiotic resistance genes. Zhao et al. [42] examined biofertilizers normally used in Chinese shrimp aquaculture systems and studied the correlation between fluoroquinolone resistance genes’ diffusion and biofertilizers. In this research project, they also screened the PMQR gene that includes: qnrA, qnrB, qnrC, qnrD, qnrS, qepA, oqxA, oqxB, and aaa(6′)-Ib genes. They screened 20 biofertilizer samples collected from shrimp farms and isolated 20 bacterial strains that were vectors of PMQR genes: 10 Escherichia coli, 9 Enterococcus faecalis, and 1 Enterococcus faecium. About 30% of biofertilizers samples presented qnrB, qnrD, and qepA resistance genes. This study was the first one which discovered the ARGs environmental repercussions due to the usage of contaminated manures on seafood farming systems. Similar patterns were also observed in terrestrial mammals, i.e., domestic swine and chicken manure (widely used in agriculture) [42]. Nowadays, there are not available data regarding finfishes, and it could be interesting to perform further investigations about possible statistical correlations between farming environments and possible agricultural implications. Therefore, these studies have confirmed ARGs diffusion and circulation in different environments through the fecal bacteria detected in common biofertilizer molecules. From these data, it can be seen that quinolones have presented reasonable risks due to the increase of their therapeutic failure. Their inclusion in the Critically Important Antimicrobials list has attracted more attention from pharma surveillance organizations.

2.2. Tetracyclines

Tetracyclines action consists of reversibly binding the 70S ribosome of cells blocking protein synthesis [3]. They are largely used in human and animal treatment as broad-spectrum antimicrobials. For the first time in Japan, it was observed that their improper administering conducted to the discovery of high nucleotide similarities of tetracycline genes between isolated bacteria from finfish aquaculture and from human clinical facilities. The phylogenetic analysis confirmed the same origin [43].
Evolution has selected different strategical and survival pathways and, in particular, four strategies: efflux pumps activation, ribosomal protection inducing a limit to the access, ribosomal RNA mutations avoiding tetracycline molecules binding, and tetracycline inactivation through enzymes [44][45]. In finfish aquaculture products, tet group responsible for proton-dependent efflux pumps encoding was mainly associated with tetracycline resistance [46]. Tet genes have been detected in several bacterial strains isolated from different animal species located in various geographical regions. There are multiple examples: tetB, tetM, tetW were firstly isolated in the intestine and rearing water of red seabream (Pagrus major) [47]; tetA, tetB, tetE, tetH, tetl, tet34, tet35 and 10 others had unknown tet genes isolated from Chilean salmon (Salmo salar) farms [48]; furthermore, Higuera-Llanten and coworkers [49] also detected the presence of tet34, tet35, tetA, tetB, tetE, tetH, tetL, and tetM genes in the same matrixes. Among seafoods (including finfish and crustaceans), Concha et al. [50] discovered tetX gene in Epilithonimonas strains from rainbow trout (Oncorhynchus mykiss) and Han et al. [51] amplified, in shrimp samples, that the tetB gene was carried in a single copy plasmid, named pTetB-VA1, comprising 5162-bp. The whole genome analysis revealed that this plasmid consists of 9 ORFs (overlapping open reading frames) encoding tetracycline-resistant repressor proteins, transcriptional regulatory proteins, and transposases and showed a 99% sequence identity to other tet gene plasmids (pIS04-68 and pAQU2). Furthermore, in terms of tet genes, with special regard to tetE, Agersø et al. [52] discovered tetE horizontal transmission between Aeromonas spp. and Escherichia coli strains, isolated from aquaculture Danish farms. TetA gene diffusion has been demonstrated to be realized through plasmids and transposons named Tn1721 and those that are Tn1721-like. Another similar example is represented by Tn5706, which is involved in tetH dissemination (amplified from Moraxella spp. and Acinetobacter spp. strains isolated from salmon farms) [53]. Due to the expanding of the AMR phenomenon among different bacterial strains, tet genes have been widely amplified from Enterobacteriaceae [54][55], Photobacterium spp., Vibrio spp., Alteromonas spp., Pseudomonas spp., and other marine commensal bacteria. Consequently, the possibility of transferring ARGs from marine microbiota to the human one is considered reasonable. Indeed, many biomolecular investigations have highlighted the possible cross-species ARGs transmission through the foodstuffs ingestion [44][56].
The wide oligonucleotide diversities, as described above, are expressions of the mass administering of tetracycline. Any mammalian zootechnic sectors (i.e., domestic swine) have improperly used this antibiotic class, inducing multiplication and genetic transmissions to the next generations of bacterial isolates (from pathogen to commensal strains, and vice versa).

2.3. Sulfonamides

In aquaculture, sulfonamides are commonly co-administered with trimethoprim, ormethoprim, and florfenicol [57]. The dihydropteroate synthase (DHPS) enzyme, in the folic acid pathway, represents the biochemical target reaction [56]. Sulfonamide’s resistance mechanisms derive from mutations in the chromosomal folP gene that provides varying degrees of trade-off between resistance and efficient folate synthesis, decreasing DHPS affinity for the antimicrobial molecule [56].
Among the discovered ARGs, four different sul gene determinants have been described to encode antibiotic resistance. Sul1 gene has been founded in class 1 integrons and linked to other resistance genes [58]; sul2 is associated with non-conjugative plasmids of the IncQ group and to large transmissible plasmids, such as pBP1 [59]. Sul3 is characterized in the Escherichia coli conjugative plasmid pVP440; sul4 gene has been recently mobilized and phylogenetic inference pinpoints its putative origin as part of the folate synthesis cluster in the Chloroflexi phylum [60]. All described ARGs have a common action, which is represented by the reduction in strategical bacterial structural expression. The transmembrane architectures are widely involved in the cyto-chemical interaction between strains and antibiotic molecules.
The genome and proteome analyses revealed that a gene cluster, containing a flavin-dependent monooxygenase and a flavin reductase, is highly upregulated in response to sulfonamides action, as reported by Kim et al. [61]. Indeed, the biochemical analysis showed that the two-components (belonging to the monooxygenase system) were key enzymes for the initial sulfonamides cleavage. It was observed that the co-expression of the two-component system in Escherichia coli conferred decreased susceptibility to sulfamethoxazole, indicating that the genes encoding drug inactivating enzymes are potential resistance determinants. Comparative genomic analysis revealed that this cluster gene, containing sulfonamide monooxygenase (renamed as sulX) and flavin reductase (sulR), is highly conserved in genomic islands. These ones are shared among sulfonamide-degrading Actinobacteria, all of which also contained sul1-carrying class 1 integrons [61].
Sulfonamide’s ARGs distribution has been widely found in numerous fish and environmental specimens, i.e., Muziasari and coworkers [62] discovered sul1, sul2, and intI1 genes detection in all analyzed samples and the dfrA1 gene in most samples in aquatic farm sediment in the Baltic Sea [63]. Domínguez et al. [64] detected sul1, sul2, class 1 integron-integrase gene intI1, dfrA1, dfrA12, and dfrA14 from a salmon farm in Chile and revealed the occurrence of transferable integrons and sul and dfr genes among sulfonamide- and/or trimethoprim-resistant bacteria, as amplified from Actinobacter spp., Bacillus spp., Proteus spp., and Pseudomanas spp. isolates [32].
These last considerations highlight that environmental stimuli can be responsible for increased or reduced ARGs transcriptions. The deduction leads to the consideration that in the AMR phenomenon, “the environment” plays a crucial role, while human and animal health are only “direct consequences”.

2.4. Thiamphenicol and Florfenicol

Thiamphenicol and florfenicol belong to the amphenicol antibiotic class and have been largely administered in aquaculture farms. Due to the possible chemical residual persistence in finfish muscular tissues, various studies have demonstrated possible sanitary implications on humans, animals, and environments [65][66].
Focusing on risk-based approach (in accordance with the EU Reg. No. 852/2004 and No. 37/2010), the European agencies EFSA and EMA published maximum residue limits and respective daily intakes for final human consumers [65].
Veterinary practitioners normally treat infectious disease (caused by, i.e., Vibrio spp., etc.) and relative possible septicemia cases using the above-mentioned molecules [67]. These have pharma-dynamic synergic effects (binding the 50S ribosomal subunit) if they were coupled with other antibiotic classes as tetracyclines. Both molecules have become widely prescribed because they have broad spectrum effects and low costs [68].
Amphenicol illegal administering has induced an intense evolutive pressure, determining the spreading of resistant strains harboring florfenicol-resistance genes (FRGs). These FRGs are plasmid determinants and have presented high genetic trades (through horizontal transmission) across different bacterial phyla, identifying strong correlations (p values < 0.05), as observed by Zeng et al. [67].
Among amplified FRGs, cat, cfr, cml, fexA, fexB, florB, and optrA have been discovered from animal origin food matrices (including finfish ones). Their biochemical actions are involved in several pathways, i.e., protein synthesis inhibition, exporter ability, methyltransferase activation, efflux pumps, etc. [69][70].
From a microbiological perspective applied to the veterinary clinical aspects, amphenicol administering has demonstrated biochemical repercussions on intestinal microbiota. It induces shifts among bacterial biodiversity acting as strong stressor [67].
This last consideration finds explanations from cyto-chemical interactions directly associated with the consequential expression of transmissible oligonucleotide sequences. Among the above-mentioned amphenicol-resistant determinants, the metagenomic technology, coupled with next generation sequencing, has identified multiple mutations on open reading frames regions, which encode resistant mechanisms, i.e., efflux pumps, new binding epitopes, etc. [66].
Innovative biomolecular technologies, combining thiamphenicol and florfenicol administering, has permitted reusearchers to reduce their respective dosages but preserve their therapeutic efficacy [71].
The notable ARGs heterogeneity and their extreme variabilities pose the basis for further diagnostic and One Health clinical challenges. Aminophenols, as with other previously mentioned antibiotic classes, are widely used in the aquaculture zootechnic sector. Therefore, it is mandatory to preserve their therapeutic actions.

3 Antibiotic Substitutions

3.1. Vaccination

FAO reports numerous administered vaccines against different bacterial or viral diseases among finfish species. The most frequently used provide seroconversion against Vibrio salmonicida, Vibrio anguillarum, Photobacterium damselae, Aeromonas salmonicida, Yersinia ruckeri, etc. [43].
Conversely, there are few vaccines for viral diseases, in which usage is highly recommended in marine finfish farms [72]. In the aquaculture farms, vaccines can be administered through different methods: injection, in bath, or through the orofecal route [43]. Injection, through the intraperitoneal route, provides powerful and durable protection, but, on the other hand, this procedure influences animal welfare, inducing a relevant stress condition. It is commonly used for Salmo salar finfish species but is not applicable for other species, i.e., Pangasius spp. and Tilapia spp. Conversely, oral administering reduces stress (due to animal handling), since animals receive immunization through food ingestion. The main difference between these two above-mentioned methods is represented by the need for large amounts of antigens in the ingestion method to obtain an adequate immunity [73]. There are contrasting opinions on vaccines’ efficacy regarding finfish farms. Usually, after vaccination, fish farmers must administer antibiotics to control infectious disease outbreaks [74]. This condition is related to an incomplete understanding of the vaccination type and the immune system’s reaction to the “antigenic stimuli”. It is improper to compare fish immune reactions with the generated response in mammalians [75].
However, in any species, such as farmed Atlantic salmons, vaccination represents an important preventive tool [43]. Farmed salmonids (Salmo salar) receive immune protection through the injection of a pentavalent vaccine against vibriosis, furunculosis, piscrickettsiosis, infectious pancreatic necrosis, and infection salmon anemia. The vaccine has permitted a reduced usage of antibiotics [75]. In tilapia’s farms, the mucosal administering route replaces the injective method. In this fish species, evidence supports a competent immune stimulation of the antigen-presenting cells (similarly to mammalians). In this way, fish farmers reduce antibiotic administering [76].
A new frontier is represented by nano-material vaccines, which use virus-like particles, immune-stimulating complexes, liposomes, polymeric, etc. These molecules drive antigens and can drive protective responses in fish. Furthermore, nanoparticles permit antigens’ release, and, for this reason, booster vaccinations are not necessary [77], but live attenuated vaccines’ employment in aquaculture is not allowed by the European Commission. Their usage has not yet been allowed due to the wide gap of knowledge concerning possible implications on human consumers [78].

3.2. Structural Improvements

Innovative production systems have become popular among fish farmers, i.e., catfish aquaculture in the USA [5]. New fish farming systems that provide more space and efficient wastewater management allow an avoidance of the large usage of antibiotic molecules [79].
Therefore, in the USA, fish farmers introduced an innovative system called “spilt-pond” to optimize fish’s sanitary conditions and productive levels. This new system is realized through the division of the traditional ponds in two areas: an algal growth basin and a fish holding area. In this way, the growth of production is allowed by the high animals’ density in the same period of production, and the reduction in antimicrobial use is due to the continuous water filtration [80]. Conversely, in Malaysia and other Asian-Pacific regions, fish are farmed by using pond culture, ex-mining pools, cement tanks, and freshwater pen culture systems. In these structures, there is low water filtration. Animal catabolites and feces remain for all productive cycles, producing a functional substrate for any bacterial species (i.e., Enterobacteriaceae) proliferation. Furthermore, in such countries of this continent (China, Vietnam, Philippines, India, etc.), the usage of antibiotics in aquaculture is not well regulated by national law [79]. Therefore, a new approach to the aquaculture systems of production is required. Indeed, Brunton et al. [81] generated a mapping system obtained through the stakeholders’ collaboration. Correlating ecological aspects to the new above-mentioned fish farms realities. It identifies hotspots and risk points related to antibiotic usage in the aquaculture food chain. The platform provides a quantitative risk analysis at different steps of production. Therefore, these maps allow researcherus to understand the molecules’ flows, ARGs, and ARB. In this way, it is possible to monitor antibiotic resistance factors. From these elaborated data, food safety authorities may program control activities through surveillance measures.

3.3. Probiotics

Probiotics have different effects on fish farming issues, i.e., they reduce animal mortality (especially at the larval stage) [82][83][84], improve animal welfare through the immune system’s stimulation, and reduce the antibiotic therapies’ necessity. Fish farmers introduce these bacteria through the finfish diet, as supplementary feed [43]. Bacillus spp. Is largely used in numerous fish farms realities for its probiotic properties. This genus can mitigate pathogenic microorganisms’ growth and can eliminate ARB [84]. These capacities are related to the bioactive peptides’ synthesis (bacteriocin) [85], but there are also nonpeptidic molecules, i.e., phospholipids, polyketides, etc., that are classified as bacteriocin [86]. Bacillus spp. produces CAMT2; this molecule is a recent example of bacteriocin that inhibits the proliferation of different bacterial strains, i.e., Vibrio spp., Staphylococcus aureus, and Listeria monocytogenes [87]. Another interesting microbiological aspect of this genus is represented by bacterial competition. It includes competition for energy (obtained from substrates), nutrients, and adhesion sites [88]. Indeed, Bacillus spp. Can rapidly colonize organic substrates with strong adhesion capacities (due to hydrophobic and steric forces) [89]. Therefore, pathogenic bacteria find an inadequate micro-environment that results in hostility to their proliferation. Furthermore, Bacillus spp. also stimulates fish’s cell-mediated immune response. Indeed, bacterial pathogens decrease their virulence because the animal host presents a resistant and competent immune system [90].
Healthy animals require few antibiotic therapies, leading to the reduction in antibiotic consumption in the next ten years [43]. Thanks to these preventive measures, different finfish species (i.e., parrotfish) have become resistant to Vibrio alginolyticus infection. These considerations are strictly related to the concept that powerful immune systems reduce pathogen bacterial proliferation [91].

References

  1. World Health Organization (WHO). Report on Second WHO Expert Meeting, Copenhagen, Denmark: Critically Important Antimicrobials for Human Medicine; Categorization for the Development of Risk Management Strategies to Contain Antimicrobial Resistance Due to Non-Human Use. 2007. Available online: https://apps.who.int/iris/bitstream/handle/10665/43765/9789241595742_eng.pdf;jsessionid=A14A12F19C1EDC617AD74724BBD65ED2?sequence=1 (accessed on 4 September 2021).
  2. Froehlich, H.E.; Runge, C.A.; Gentry, R.R.; Gaines, S.D.; Halpern, B.S. Comparative terrestrial feed and land use of aquaculture-dominant world. Proc. Nat. Acad. Sci. USA 2018, 115, 5295–5300.
  3. Food and Agriculture Organization (FAO). Approved Drugs for Use in Seafoods; FAO: Rome, Italy, 2020; Available online: http://www.fao.org/3/ca9229en/ca9229en.pdf (accessed on 12 March 2021).
  4. Diana, J.S.; Egna, H.S.; Chopin, T.; Peterson, M.S.; Cao, L.; Pomeroy, R.; Verdegem, M.; Slack, W.T.; Bondad-Reantaso, M.G.; Cabello, F. Responsible aquaculture in 2050: Valuing local conditions and human innovations will be key to success. BioScience 2013, 6, 255–262.
  5. Chuah, L.O.; Effarizah, M.E.; Goni, A.M.; Rusul, G. Antibiotic application and emergence of multiple antibiotic resistance (MAR) in global catfish aquaculture. Curr. Environ. Health Rep. 2016, 3, 118–127.
  6. Oyinlola, M.A.; Reygondeau, G.; Wabnitz, C.; Frölicher, T.L.; Lam, V.; Cheung, W. Projecting global mariculture production and adaptation pathways under climate change. Glob. Chang. Biol. 2022, 28, 1315–1331.
  7. Liu, X.; Steele, J.C.; Meng, X.Z. Usage, Residue, and Human Health Risk of Antibiotics in Chinese Aquaculture: A Review. Environ. Pollut. 2017, 223, 161–169.
  8. Igbinosa, I.H.; Igbinosa, E.O.; Okoh, A.I. Molecular detection of metallo-β-lactamase and putative virulence genes in environmental isolates of Pseudomonas species. Pol. J. Environ. Stud. 2014, 23, 2327–2331. Available online: http://www.pjoes.com/pdf-89415-23293?filename=Molecular%20Detection%20of.pdf (accessed on 19 June 2022).
  9. Ferri, M.; Ranucci, E.; Romagnoli, P.; Giaccone, V. Book Antibiotico-Resistenza: Una Minaccia Globale per la Sanità Pubblica e i Sistemi Sanitari; Chapter 2; Piano Prevenzione 2014–2018 ASL Roma 1; 2017 Crit. Rev. Food Sci. Nutr. Available online: https://www.veterinariapreventiva.it/wp-content/uploads/2019/11/027-050_CAPITOLO-2.2.pdf (accessed on 3 March 2022).
  10. Devarajan, N.; Laffite, A.; Mulaji, C.K.; Otamonga, J.P.; Mpiana, P.T.; Mubedi, J.I.; Prabakar, K.; Ibelings, B.W.; Pote, J. Occurrence of antibiotic resistance genes and bacterial markers in a tropical river receiving hospital and urban wastewaters. PLoS ONE 2016, 11, e0149211.
  11. Nnadozie, C.F.; Odume, O.N. Freshwater environments as reservoirs of antibiotic resistant bacteria and their role in the dissemination of antibiotic resistance genes. Environ. Pollut. 2019, 254, 113067.
  12. Piedra-Carrasco, N.; Fàbrega, A.; Calero-Cáceres, W.; Cornejo-Sánchez, T.; Brown-Jaque, M.; Mir-Cros, A.; Muniesa, M.; González-López, J.J. Carbapenemase-producing Enterobacteriaceae recovered from a Spanish river ecosystem. PLoS ONE 2017, 12, e0175246.
  13. Szekeres, E.; Chiriac, C.M.; Baricz, A.; Szőke-Nagy, T.; Lung, I.; Soran, M.L.; Rudi, K.; Dragos, N.; Coman, C. Investigating antibiotics, antibiotic resistance genes, and microbial contaminants in groundwater in relation to the proximity of urban areas. Environ. Pollut. 2018, 236, 734–744.
  14. Reverter, M.; Sarter, S.; Caruso, D.; Avarre, J.C.; Combe, M.; Pepey, E.; Pouyaud, L.; Vega-Heredía, S.; de Verdal, H.; Gozlan, R.E. Aquaculture at the crossroads of global warming and antimicrobial resistance. Nat. Commun. 2020, 11, 1870.
  15. Ginovyan, M.; Hovsepyan, V.; Sargsyan, M.; Grigoryan, K.; Trchounian, A. Antibiotic resistance of Pseudomonas species isolated from Armenian fish farms. Process Union Res Inst Marine Fish Oceanograph 2017, 167, 163–173. Available online: http://aquacultura.org/upload/files/pdf/library/trudy/167-20.pdf (accessed on 22 March 2022).
  16. Sacramento, A.G.; Fernandes, M.R.; Sellera, F.P.; Dolabella, S.S.; Zanella, R.C.; Cerdeira, L.; Lincopan, N. VanA-type vancomycin-resistant Enterococcus faecium ST1336 isolated from mussels in an anthropogenically impacted ecosystem. Marine Pollut. Bull. 2019, 142, 533–536.
  17. Ferreira, A.; Pavelquesi, S.; Monteiro, E.; Rodrigues, L.; Silva, C.; Silva, I.; Orsi, D.C. Prevalence and Antimicrobial Resistance of Salmonella spp. in Aquacultured Nile Tilapia (Oreochromis niloticus) Commercialized in Federal District, Brazil. Foodborne Pathog. Dis. 2021, 18, 778–783.
  18. Araújo, A.; Grassotti, T.T.; Frazzon, A. Characterization of Enterococcus spp. isolated from a fish farming environment in southern Brazil. Brazil. J. Biol. 2021, 81, 954–961.
  19. Fu, H.; Yu, P.; Liang, W.; Kan, B.; Peng, X.; Chen, L. Virulence, Resistance, and Genomic Fingerprint Traits of Vibrio cholerae Isolated from 12 Species of Aquatic Products in Shanghai, China. Microb. Drug Res. 2020, 26, 1526–1539.
  20. Feng, Y.; Bai, M.; Geng, Y.; Chen, D.; Huang, X.; Ouyang, P.; Guo, H.; Zuo, Z.; Huang, C.; Lai, W. The potential risk of antibiotic resistance of Streptococcus iniae in sturgeon cultivation in Sichuan, China. Environ. Sci. Pollut. Res. Int. 2021, 28, 69171–69180.
  21. Zhu, W.; Zhou, S.; Chu, W. Comparative proteomic analysis of sensitive and multi-drug resistant Aeromonas hydrophila isolated from diseased fish. Microb. Pathog. 2020, 139, 103930.
  22. Preena, P.G.; Dharmaratnam, A.; Swaminathan, T.R. Antimicrobial Resistance analysis of Pathogenic Bacteria Isolated from Freshwater Nile Tilapia (Oreochromis niloticus) Cultured in Kerala, India. Cur. Microbiol. 2020, 77, 3278–3287.
  23. Basha, K.A.; Kumar, N.R.; Das, V.; Reshmi, K.; Rao, B.M.; Lalitha, K.V.; Joseph, T.C. Prevalence, molecular characterization, genetic heterogeneity and antimicrobial resistance of Listeria monocytogenes associated with fish and fishery environment in Kerala, India. Lett. Appl. Microbiol. 2019, 69, 286–293.
  24. Labella, A.; Gennari, M.; Ghidini, V.; Trento, I.; Manfrin, A.; Borrego, J.J.; Lleo, M.M. High incidence of antibiotic multi-resistant bacteria in coastal areas dedicated to fish farming. Marine Pollut. Bull. 2013, 70, 197–203.
  25. Nguyen, H.N.; Van, T.T.; Nguyen, H.T.; Smooker, P.M.; Shimeta, J.; Coloe, P.J. Molecular characterization of antibiotic resistance in Pseudomonas and Aeromonas isolates from catfish of the Mekong Delta, Vietnam. Vet. Microbiol. 2014, 171, 397–405.
  26. Boss, R.; Overesch, G.; Baumgartner, A. Antimicrobial Resistance of Escherichia coli, Enterococci, Pseudomonas aeruginosa, and Staphylococcus aureus from Raw Fish and Seafood Imported into Switzerland. J. Food Protect. 2016, 79, 1240–1246.
  27. Koudou, A.A.; Kakou-Ngazoa, S.; Konan, K.F.; Aka, E.; Addablah, A.; Coulibaly N’Golo, D.; Kouassi, S.; Sina, M.K.; Atta Diallo, H.; Guessend, N.; et al. Occurrence of multidrug-resistant bacteria in aquaculture farms in Côte d’Ivoire (West Africa). Afr. J. Microbiol. Res. 2020, 14, 182–188. Available online: https://academicjournals.org/journal/AJMR/article-full-text-pdf/D4E869B63678 (accessed on 2 July 2022).
  28. Rezai, R.; Ahmadi, E.; Salimi, B. Prevalence and Antimicrobial Resistance Profile of Listeria Species Isolated from Farmed and On-Sale Rainbow Trout (Oncorhynchus mykiss) in Western Iran. J. Food Protect. 2018, 81, 886–891.
  29. Miranda, C.D.; Godoy, F.A.; Lee, M.R. Current status of the use of antibiotics and the antimicrobial resistance in the Chilean salmon farms. Front. Microbiol. 2018, 9, 1284.
  30. Colquhoun, D.J.; Aarflot, L.; Melvold, C.F. gyrA and parC mutations and associated quinolone resistance in Vibrio anguillarum serotype O2b strains isolated from farmed Atlantic cod (Gadus morhua) in Norway. Antimicrob. Agents Chemother. 2007, 51, 2597–2599.
  31. Izumi, S.; Ouchi, S.; Kuge, T.; Arai, H.; Mito, T.; Fujii, H. PCR–RFLP genotypes associated with quinolone resistance in isolates of Flavobacterium psy- chrophilum. J. Fish Dis. 2007, 30, 141–147.
  32. Shah, S.Q.; Nilsen, H.; Bottolfsen, K.; Colquhoun, D.J.; Sørum, H. DNA gyrase and topoisomerase IV mutations in quinolone-resistant Flavobacterium psychrophilum isolated from dis- eased salmonids in Norway. Microb. Drug Res. 2012, 18, 207–214.
  33. Lukkana, M.; Wongtavatchai, J.; Chuanchuen, R. Class 1 integrons in Aeromonas hydrophila isolates from farmed Nile tilapia (Oreochromis nilotica). J. Vet. Med. Sci. 2012, 74, 435–440.
  34. Goñi-Urriza, M.; Arpin, C.; Capdepuy, M.; Dubois, V.; Caumette, P.; Quentin, C. Type II topoisomerase quinolone resistance- determining regions of Aeromonas caviae, A. hydrophila and A. sobria complexes and mutations associated with quinolone resistance. Antimicrob. Agents Chemother. 2002, 46, 350–359.
  35. Kim, S.R.; Nonaka, L.; Suzuki, S. Occurrence of tetracycline resistance genes tet(M) and tet(S) in bacteria from marine aqua- culture sites. FEMS Microbiol. 2004, 237, 147–156.
  36. Pepi, M.; Focardi, S. Antibiotic-Resistant Bacteria in Aquaculture and Climate Change: A Challenge for Health in the Mediterranean Area. Int. J. Environ. Res. Public Health 2021, 18, 5723.
  37. Yan, L.; Liu, D.; Wang, X.H.; Wang, Y.; Zhang, B.; Wang, M.; Xu, H. Bacterial plasmid-mediated quinolone resistance genes in aquatic environments in China. Sci. Rep. 2017, 7, 40610.
  38. Jiang, H.; Tang, D.; Liu, Y.; Zhang, X.; Zeng, Z.; Xu, L.; Hawkey, P. Prevalence and characteristics of β-lactamase and plasmid-mediated quinolone resistance genes in Escherichia coli isolated from farmed fish in China. J. Antimicrob. Chemother. 2012, 67, 2350–2353.
  39. Dobiasova, H.; Kutilova, I.; Piackova, V.; Vesely, T.; Cizek, A.; Dolejska, M. Ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids. Vet. Microbiol. 2014, 171, 413–421.
  40. Mukwabi, D.M.; Okemo, P.O.; Otieno, S.A.; Oduor, R.O.; Okwany, Z.W. Antibiotic Resistant Pathogenic Bacteria Isolated from Aquaculture System in Bungoma County, Kenya. J. Appl. Environ. Microbioliol. 2019, 7, 25–37. Available online: https://ir-library.ku.ac.ke/bitstream/handle/123456789/21128/Antibiotic%20resistant%20pathogenic%20bacteria%20isolated%20from%20Aquaculture%20systems.pdf?sequence=1 (accessed on 3 March 2022).
  41. Heuer, H.; Schmitt, H.; Smalla, K. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 2011, 14, 236–243.
  42. Zhao, S.; Wei, W.; Fu, G.; Zhou, J.; Wang, Y.; Li, X.; Ma, L.; Fang, W. Application of biofertilizers increases fluoroquinolone resistance in Vibrio parahaemolyticus isolated from aquaculture environments. Marine Pollut. Bull. 2020, 150, 110592.
  43. Food and Agriculture Organization (FAO). The State of World Fisheries and Aquaculture 2018. Meeting the Sustainable Development Goals; FAO: Rome, Italy, 2018; Available online: http://www.fao.org/3/i9540en/i9540en.pdf (accessed on 7 June 2021).
  44. Speer, B.S.; Shoemaker, N.B.; Salyers, A.A. Bacterial resistance to tetracycline: Mechanisms, transfer, and clinical significance. Clin. Microbiol. Rev. 1992, 5, 387–399.
  45. Taylor, D.E.; Chau, A. Tetracycline resistance mediated by ribosomal protection. Antimicrob. Agents Chemother. 1996, 40, 1–5.
  46. Roberts, M.C.; Schwarz, S.; Aarts, H.J.M. Erratum: Acquired antibiotic resistance genes: An overview. Front. Microbiol. 2012, 3, 384.
  47. Obayashi, Y.; Kadoya, A.; Kataoka, N.; Kanda, K.; Bak, S.M.; Iwata, H.; Suzuki, S. Tetracycline Resistance Gene Profiles in Red Seabream (Pagrus major) Intestine and Rearing Water After Oxytetracycline Administration. Front. Microbiol. 2020, 11, 1764.
  48. Roberts, M.C.; No, D.; Kuchmiy, E.; Miranda, C.D. Tetracycline resistance gene tet(39) identified in three new genera of bacteria isolated in 1999 from Chilean salmon farms. J. Antimicrob. Chemother. 1999, 70, 619–621.
  49. Higuera-Llante´n, S.; Va´squez-Ponce, F.; Barrientos-Espinoza, B.; Mardones, F.O.; Marshall, S.H.; Olivares-Pacheco, J. Extended antibiotic treatment in salmon farms select multiresistant gut bacteria with a high prevalence of antibiotic resistance genes. PLoS ONE 2018, 13, e0203641.
  50. Concha, C.; Miranda, C.D.; Santander, J.; Roberts, M.C. Genetic Characterization of the Tetracycline Resistance Gene tet(X) Carried by Two Epilithonimonas Strains Isolated from Farmed Diseased Rainbow Trout, Oncorhynchus mykiss in Chile. Antibiotics 2021, 10, 1051.
  51. Han, J.E.; Mohney, L.L.; Tang, K.F.J.; Pantoja, C.R.; Lightner, D.V. Plasmid mediated tetracycline resistance of Vibrio parahaemolyticus associated with acute hepatopancreatic necrosis disease (AHPND) in shrimps. Aquacul. Rep. 2015, 2, 17–21.
  52. Agersø, Y.; Bruun, M.S.; Dalsgaard, I.; Larsen, J.L. The tetracycline resistance gene tet(E) is frequently occurring and present on large horizontally transferable plas- mids in Aeromonas spp. from fish farms. Aquaculture 2007, 266, 47–52.
  53. Miranda, C.D.; Kehrenberg, C.; Ulep, C.; Schwarz, S.; Roberts, M.C. Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrob. Agents Chemother. 2003, 47, 883–888.
  54. Su, H.C.; Ying, G.G.; Tao, R.; Zhang, R.Q.; Fogarty, L.R.; Kolpin, D.W. Occurrence of antibiotic resistance and characterization of resistance genes and integrons in Enterobacteriaceae isolated from integrated fish farms in South China. J. Environ. Monit. 2011, 13, 3229–3236.
  55. Gao, P.; Mao, D.; Luo, Y.; Wang, L.; Xu, B.; Xu, L. Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res. 2012, 46, 2355–2364.
  56. Sørum, H. Antimicrobial drug resistance in fish pathogens. In Antimicrobial Resistance in Bacteria of Animal Origin; Wiley Online Library: Hoboken, NJ, USA, 2006; pp. 213–238.
  57. Serrano, P.H. Responsible Use of Antibiotics in Aquaculture; FAO Fisheries Technical Paper; FAO: Rome, Italy, 2005; p. 469. Available online: https://books.google.it/books?hl=it&lr=&id=f3Eql-OUOrAC&oi=fnd&pg=PR9&dq=Responsible+use+of+antibiotics+in+aquaculture&ots=by9D2xmv0K&sig=7LtKD2EFrqNSS8spEK5nA1pAVho&redir_esc=y#v=onepage&q=Responsible%20use%20of%20antibiotics%20in%20aquaculture&f=false (accessed on 2 March 2021).
  58. Rådström, P.; Swedberg, G.; Sköld, O. Genetic analyses of sulfonamide resistance and its dissemination in gram-negative bacteria illustrate new aspects of R plasmid evolution. Antimicrob. Agents Chemother. 1991, 35, 1840–1848.
  59. Enne, V.I.; Livermore, D.M.; Stephens, P.; Hall, L.M. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 2001, 357, 1325–1328.
  60. Nakayama, T.; Tran, T.T.H.; Harada, K.; Warisaya, M.; Asayama, M.; Hinenoya, A.; Lee, J.W.; Phu, T.M.; Ueda, S.; Sumimura, Y. Water metagenomic analysis reveals low bacterial diversity and the presence of antimicrobial residues and resistance genes in a river containing wastewater from backyard aquacultures in the Mekong Delta, Vietnam. Environ. Pollut. 2017, 222, 294–306.
  61. Kim, D.W.; Thawng, C.N.; Lee, K.; Wellington, E.M.H.; Cha, C.J. A novel sulfonamide resistance mechanism by two-component flavin-dependent monooxygenase system in sulfonamide-degrading actinobacteria. Environ. Int. 2019, 127, 206–215.
  62. Muziasari, W.I.; Managaki, S.; Pärnänen, K.; Karkman, A.; Lyra, C.; Tamminen, M. Sulfonamide and Trimethoprim Resistance Genes Persist in Sediments at Baltic Sea Aquaculture Farms but Are Not Detected in the Surrounding Environment. PLoS ONE 2014, 9, e92702.
  63. Muziasari, W.I.; Pitkanen, L.K.; Sørum, H.; Stedtfeld, R.D.; Tiedje, J.M.; Virta, M. The resistome of farmed fish feces contributes to the enrichment of antibiotic resistance genes in sediments below Baltic Sea fish farms. Front. Microbiol. 2017, 7, 2137.
  64. Domínguez, M.; Miranda, C.D.; Fuentes, O.; de la Fuente, M.; Godoy, F.A.; Bello-Toledo, H.; González-Rocha, G. Occurrence of Transferable Integrons and sul and dfr Genes Among Sulfonamide-and/or Trimethoprim-Resistant Bacteria Isolated From Chilean Salmonid Farms. Front. Microbiol. 2019, 10, 748.
  65. Schar, D.; Klein, E.Y.; Laxminarayan, R.; Gilbert, M.; Van Boeckel, T.P. Global trends in antimicrobial use in aquaculture. Sci. Rep. 2020, 10, 21878.
  66. Jung, H.N.; Park, D.H.; Choi, Y.J.; Kang, S.H.; Cho, H.J.; Choi, J.M.; Shim, J.H.; Zaky, A.A.; Abd El-Aty, A.M.; Shin, H.C. Simultaneous Quantification of Chloramphenicol, Thiamphenicol, Florfenicol, and Florfenicol Amine in Animal and Aquaculture Products Using Liquid Chromatography-Tandem Mass Spectrometry. Front. Nutr. 2022, 8, 812803.
  67. Zeng, Q.; Liao, C.; Terhune, J.; Wang, L. Impacts of florfenicol on the microbiota landscape and resistome as revealed by metagenomic analysis. Microbiome 2019, 7, 155.
  68. Xie, X.; Wang, B.; Pang, M.; Zhao, X.; Xie, K.; Zhang, Y.; Wang, Y.; Guo, Y.; Liu, C.; Bu, X.; et al. Quantitative analysis of chloramphenicol, thiamphenicol, florfenicol and florfenicol amine in eggs via liquid chromatography-electrospray ionization tandem mass spectrometry. Food Chem. 2018, 269, 542–548.
  69. Wang, Y.; Lv, Y.; Cai, J.; Schwarz, S.; Cui, L.; Hu, Z.; Zhang, R.; Li, J.; Zhao, Q.; He, T.; et al. A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin. J. Antimicrob. Chemother. 2015, 70, 2182–2190.
  70. Figueroa, J.; Castro, D.; Lagos, F.; Cartes, C.; Isla, A.; Yáñez, A.J.; Avendaño-Herrera, R.; Haussmann, D. Analysis of single nucleotide polymorphisms (SNPs) associated with antibiotic resistance genes in Chilean Piscirickettsia salmonis strains. J. Fish Dis. 2019, 42, 1645–1655.
  71. Assaneab, I.M.; Suemi, K.; Moraes, G.G.; Valladãoac, R.; Pilarskia, F. Combination of antimicrobials as an approach to reduce their application in aquaculture: Emphasis on the use of thiamphenicol/florfenicol against Aeromonas hydrophila. Aquaculture 2019, 507, 238–245.
  72. Rodger, H.D. Fish Disease Causing Economic Impact in Global Aquaculture. In Fish Vaccines. Birkhäuser Advances in Infectious Diseases; Adams, A., Ed.; Springer: Basel, Switzerland, 2016; Available online: https://link.springer.com/chapter/10.1007/978-3-0348-0980-1_1 (accessed on 3 March 2022).
  73. Lakshmi, B.; Syed, S.; Buddolla, V. Chapter 10—Current advances in the protection of viral diseases in aquaculture with special reference to vaccination. In Recent Developments in Applied Microbiology and Biochemistry; Elsevier: Amsterdam, The Netherlands, 2019; pp. 127–146.
  74. Center for Disease Control and Prevention (CDC). Get Smart: Know when Antibiotics Work; Center for Disease Control: Atlanta, GA, USA, 2010; Available online: https://apua.org/cdc-get-smart-week (accessed on 12 May 2022).
  75. Flores-Kossack, C.; Montero, R.; Köllner, B.; Maisey, K. Chilean aquaculture and the new challenges: Pathogens, immune response, vaccination and fish diversification. Fish Shellfish Immunol. 2020, 98, 52–67.
  76. Munang’andu, H.M.; Mutoloki, S.; Evensen, Ø.A. Review of the Immunological Mechanisms Following Mucosal Vaccination of Finfish. Front. Immunol. 2015, 6, 427.
  77. Ji, J.; Torrealba, D.; Ruyra, À.; Roher, N. Nanodelivery Systems as New Tools for Immunostimulant or Vaccine Administration: Targeting the Fish Immune System. Biology 2015, 4, 664–696.
  78. Brudeseth, B.E.; Wiulsrød, R.; Fredriksen, B.N.; Lindmo, K.; Løkling, K.E.; Bordevik, M.; Steine, N.; Klevan, A.; Gravningen, K. Status and future perspectives of vaccines for industrialised fin-fish farming. Fish Shellfish Immunol. 2013, 35, 1759–1768.
  79. Food and Agriculture Organization (FAO). Search Aquacultured Fact Sheets: Cultured Aquatic Species. 2016. Available online: http://www.fao.org/fishery/culturedspecies/search/en (accessed on 18 February 2021).
  80. United States Department of Agriculture (UNDA). Performance Evaluation of Intensive, Pond-Based Culture Systems for Catfish Production; Southern Regional Aquaculture Center (USA, New York): 2014. Available online: https://srac.msstate.edu/pdfs/APRS%20and%20Summary/27th%20APR%20web-%20indivual%20reports/Intensive%20Systems%20CR%20for%202014.pdf (accessed on 2 February 2022).
  81. Brunton, L.A.; Desbois, A.P.; Garza, M.; Wieland, B.; Mohan, C.V.; Häsler, B.; Tam, C.C.; Le, P.; Phuong, N.T.; Van, P.T.; et al. Identifying hotspots for antibiotic resistance emergence and selection, and elucidating pathways to human exposure: Application of a systems-thinking approach to aquaculture systems. Sci. Total Environ. 2019, 687, 1344–1356.
  82. Lauzon, H.L.; Gudmundsdottir, S.; Steinarsson, A.; Oddgerisson, M.; Peturdottir, S.K.; Reynisson, E.; Bjorndottir, R.; Gudumundsdottir, B.K. Effects of bacterial treatment at early stages of Atalntic cod (Gadus morhua L.) on larval survival and development. J. Appl. Microbiol. 2010, 108, 624–632.
  83. Makridis, P.; Martins, S.; Reis, J.; Dinis, M.T. Use of probiotic bacteria in the rearing of Senegalese sole (Solea senegalensis) larvae. Aquacul. Res. 2008, 39, 627–634.
  84. Plante, S.; Pernet, F.; Hache, R.; Ritchie, R.; Ji, B.J.; McIntosh, D. Ontogenetic variations in lipid class and fatty acid composition of haddock larvae Melanogrammus aeglefinus in relation to changes in diet and microbial environment. Aquaculture 2007, 263, 107–121.
  85. Zou, J.; Jiang, H.; Cheng, H.; Fang, J.; Huang, G. Strategies for screening, purification and characterization of bacteriocins. Int. J. Biol. Macromol. 2018, 117, 781–789.
  86. Stein, T. Bacillus subtilis antibiotics: Structures, syntheses and specific functions. Mol. Microbiol. 2005, 56, 845–857.
  87. An, J.; Zhu, W.; Liu, Y.; Zhang, X.; Sun, L.; Hong, P.; Wang, Y.; Xu, C.; Liu, H. Purification and characterization of a novel bacteriocin CAMT2 produced by Bacillus amyloliquefaciens isolated from marine fish Epinephelus areolatus. Food Control 2015, 51, 278–282.
  88. Food and Drug Administration (FDA). Approved Drugs for Use in Seafoods; FDA:, New York. 2020. Available online: https://www.fda.gov/animal-veterinary/aquaculture/approved-aquaculture-drugs (accessed on 1 June 2021).
  89. Mohapatra, S.; Chakraborty, T.; Kumar, V.; DeBoeck, G.; Mohanta, K.N. Aquaculture and stress management: A review of probiotic intervention. J. Animal Physiol. Animal Nutr. 2013, 97, 405–430.
  90. Wilson, A.B. MHC and adaptive immunity in teleost fishes. Immunogen 2017, 69, 521–528.
  91. Yang, Y.; Zeng, G.; Huang, D.; Zhang, C.; He, D.; Zhou, C.; Wang, W. Molecular Engineering of Polymeric Carbon Nitride for Highly Efficient Photocatalytic Oxytetracycline Degradation and H2O2 Production. Appl. Catal. Environ. 2020, 272, 118970.
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