Food safety in fisheries: Application of One Health approach

Microbial issues

Foods, particularly of animal origin (meat, milk, eggs, and fish) support the growth of microbes (bacteria, viruses, and parasites) that can serve as potential sources of food-borne illnesses. Although viruses are grossly accounted for the majority of food-borne illnesses, but hospitalisation and mortality rates are associated either due to bacterial agents or their toxins. The illnesses may range from mild gastroenteritis to neurological, hepatic, and renal syndromes. It has been reported that more than 90 per cent of food-borne illnesses are due to various species of Staphylococcus aureus, Escherichia coli, Salmonella spp., Listeria, Vibrio, Clostridium, and Campylobacter1273.

In aquaculture, bacteria, viruses, and trematodes are the major biological hazards73. The bacterial agents of public health importance that can contaminate aquaculture and its products are broadly divided into two viz., indigenous microbiota i.e., those which are naturally present in the aquaculture environment (C. botulinum, V. parahaemolyticus, V. cholerae, Aeromonas, Listeria) and non-indigenous microflora i.e., those introduced into the environment by way of excreta (Salmonella spp. and E. coli). Intensive aquaculture practices have promoted the growth of several bacterial infections (E. coli, Salmonella spp., Shigella spp., Aeromonas hydrophila, V.parahaemolyticus, V.cholerae, V. vulnificus, Plesiomonas shigelloides, Edwardsiella tarda, and Streptococcus iniae), which would lead to increased use of antimicrobials141516171819202122. However, it is not easy to determine the levels of antimicrobial usage in aquaculture as the quantum and compounds put in practice differ significantly among countries. Consequently, antimicrobials would be employed in aquaculture therapeutically, prophylactically, and metaphylactically not only to manage the infections but also to promote growth23.

The surge in the food-borne infections caused by drug-resistant bacteria was correlated with the antibiotic usage in food animals and the emergence of resistant infections among humans and animal pathogens. Such drug-resistant pathogens could be directed to the human food chain either by way of direct contact (aquatic biota or drinking water), or through the consumption of contaminated seafood. Furthermore, the antibiotic selection pressure alters the biodiversity of the aquatic environment and commensal flora of aquatic biota23242526. Additionally, the exchange of genetic material may take place between the aquatic and terrestrial bacterial pathogens on exposing the terrestrial bacteria in the aquatic environment to residual antimicrobials and biofilm. This fact could be evidenced by the sharing of genetic material and resistance determinants for antibiotics such as beta-lactamases, tetracyclines, and quinolones between aquatic bacteria, fish pathogens as well as human pathogens73.

The concern over antimicrobial usage in aquaculture could be aggravated with the incidence of antimicrobial residues in aquatic species. The antibiotics could accumulate as residues in tissues, even before these are metabolised wholly or excreted from the system. This can occur when the aquatic species are harvested for consumption while on medication or before the appropriate withdrawal period. Such cases of residues in aquaculture products have been reported from countries like India23, Bangladesh24, Nigeria25, and Iran26. The occurrence of antimicrobial residues has raised apprehensions over the recent years owing to public health concerns (drug resistance, hypersensitivity, mutagenicity, carcinogenicity, teratogenicity, aplastic anaemia, and dysbiosis of commensal gut flora) among seafood merchandise23242526.

Besides bacteria, a wide range of fish species harbour parasites; some of them are highly pathogenic and are transmitted by way of consumption of raw and inadequately cooked fish. In general, fish serves as intermediate hosts for these parasites; humans act as a definitive host when the infectious stages are consumed. Such parasitic infections are more often prevalent in those communities which prefer eating raw or undercooked fish, mainly in eastern and southern Asia2728. Freshwater fisheries are commonly associated with parasitic infections; little is known about the role of farmed aquaculture species. The two major genera of medical importance include Chlonorchis and Opisthorchis; Paragonimus, Heterophyes, and Metagonimus are of lesser importance272829303132.

Apart from bacterial and parasitic infections, viruses (commonly norovirus, and hepatitis viruses types- A and E) are also associated with disease outbreaks343536. Contamination of aquaculture species, especially the bivalves occur from the discharges of sewage effluents, urban runoff, and wastes from boats and through animal sources. Viral contamination is regarded as a public health hazard and hampers sustainable aquaculture practices. The issue attains complication as the current risk assessment and regulations rely only on bacterial indicators (predominantly, coliforms, E. coli, and faecal streptococci) for the detection of faecal pollution in aquaculture. Such bacterial indicators could not represent the public health risk of aquaculture from enteric viral pathogens34353644.

Chemical issues

Chemical additives (colourants and preservatives) and contaminants (heavy metal, pesticide, and antibiotic residues) have been found plentiful in foods. These agents often used to eradicate and control vermins, are found in the foods and associated environment. Besides, biotoxins such as mycotoxins, marine biotoxins, cyanogenic glycosides can enter the food chain causing impairment in the immune system and can lead to cancer3738.

In countries where aquaculture forms the backbone, a plethora of chemicals (antibiotics, pesticides, disinfectants, and water conditioners) are employed to sustain the production. Such strategies would not only lead to the emergence of antimicrobial resistance, particularly, multi-drug resistance but also tend to infect the non-target species. Such chemicals could turn out to be disruptive and find their way into the natural ecosystem that would eventually lead to irreparable damage to the aquatic system38. Plastics (often micro-and nano- plastics) resulting from the degradation and fragmentation of larger plastic items may enter the aquatic matrices (surface, sediments, beaches, etc.). Even though removal of the gastrointestinal tract of seafood would alleviate the risk of microplastics in humans, consumption of these aquatic species (bivalves and small fish) wholly may result in microplastic exposure. However, their fate in the human gastrointestinal tract is not completely understood1.

Environmental hygiene issues

The most important element determining the aquacultural microflora is its environment7. Improper disposal and recycling facilities in food-producing and processing plants would lead to an increased risk of the pest as well as insect population, resulting in food spoilage and contamination. The water temperature, harvesting techniques, season, and processing methods may also influence the spoilage. The predominant bacterial spoilage agents are located on the slime layer of the skin, gills, and intestine. As the tissues of fish contain higher levels of non-protein nitrogenous (NPN) compounds (trimethylamine oxide, free amino acids, and creatinine), proteins, and peptides, the growth of microbes results in the decomposition of proteins and production of metabolites which would result in spoilage.

Waste thrown away from the food industries into the environment is a cause of public health concern. Besides routine chemicals (antimicrobials, pesticides, hormones, pigments, minerals, vitamins), persistent organic pollutants (POPs) such as dioxins and polychlorinated biphenyls (PCBs) are found in the environment abundantly and accumulate in animal food chains3940. Similarly, heavy metals (lead, cadmium, mercury) could pave their way in foods mainly through pollution of air, water, and soil414243.

Inappropriate aquacultural practices could result in environmental degradation; eutrophication and organic pollution constitute common adverse impacts. Together with chemical pollution, these could deplete oxygen, reduce water quality, coral death, and habitat disruption of water bodies. Such a hostile environment would sustain the growth of harmful microbes to aquatic life73.

Personal hygiene issues

Inadequate personal hygiene of the handlers poses significant occupational as well as a public health risk. Alike, clean water and water body, harvest equipment, and containers would suffice the public health risks, if any, that would culminate in foodborne illnesses. Since the disease outbreaks of public health concern could seldom be correlated to the disease manifestation in fishes, intervention approaches for assuring food safety in aquaculture practices are quite difficult to be determined. Therefore, quantitative risk assessment is considered to be the best method for identifying pathogens. The quantitative risk assessment criteria employed for the pathogen identification involve the formulation of the problem, assessment of exposure as well as health effects, and finally, the risk characterization. Often, stochastic techniques such as Monte Carlo modelling could also be devised as suitable microbial quantitative risk assessment methods74. The data thus generated, could be used in arriving at decisions during risk management, and employed for effective implementation of hazard analysis and a critical control point (HACCP)- based food safety assurance programmes. Although the concept of ‘farm-to-fork’ has progressed in the aquaculture processing sector, yet its application in farming to ensure food safety remains still in infancy12.

Human health

In general, food production systems can provide a wide range of public health as well as socio-economic benefits. The OH principles can achieve investment and optimization towards productivity, welfare concerns, and ecosystem health. Practically, the market preferences or societal goals to tolerate health will play a crucial role. The ever-increasing population, as well as urbanising trends in the human population, may compromise the accessibility and nutritive quality of natural foods; therefore, the processed foods are of utmost importance. Aquaculture enterprises can solve this issue to a greater extent by providing locally available nutritious foods mainly in low- and middle-income countries (LMICs), thereby opening up employment avenues to many1276. In short, scope for trade, opportunities for better employability, quality diet and better infrastructural facilities determine the success metrics of aquaculture. Moreover, a safe supply chain (farm- to- fork) is imperative to alleviate the burden of public health impacts and to enhance the economic stability of the society and nation. Hence, access to an optimum quantity of safe and nutritive food is pivotal for the sustenance of life, promoting better health and thereby stabilising the economy75.

While public health threats are emerging, early evaluation of such risks is essential to uphold the OH principles. For instance, the escalating international trade has impacted the bivalve mollusc production ever since the 1950s, the dearth in the framework, availability of the origin, occurrence, and characterized data of those pathogens of public health significance in the aquatic ecosystems have underestimated the supply chain demands and exports from LMICs75.

Organism health

Food production involves complex socio-ecological systems within an environment with a wide variety of species habitat. Farmed macrobiotic communities interact often with a wide range of eukaryotic as well as prokaryotic microbes inside the aquatic environment. Within the aquatic ecosystem involves a variety of known and unknown pathogens that may produce infection and disease. Hence, the crop-growing water bodies are regarded as artificial ecosystems that can act as a conducive environment for rapid propagation of pathogens and emergence of public health outbreaks6. It is therefore, important to consider the stock management in terms of public health aspects, particularly biosecurity, zoonoses, therapeutic and/or interventional impact on the limited aquatic environment.

The intensive aquacultural practices have necessitated the use of chemicals (pond fertilizers, biocides, chemotherapeutics, and formulaic feeds) for improving stock performance. On the research front, microbial identification and hazard profiling employing sophisticated technologies such as metagenomic analysis or next-generation sequencing of water bodies, feed, and host tissues are attracting wide momentum. Such technological advancements could not only identify the biosecurity risks associated with aquaculture but also prevent the pathogen spillover to the adjoining environment and wildlife per se7576.

Environmental health

The majority of aquaculture enterprise is fresh water-based, and the rest is based on marine and brackish habitats. However, drastic climatic changes have resulted in the heating up of water bodies and the expansion of hypoxic zones affecting the marine ecosystem77. Culture platforms for aquatic species (bivalves and seaweeds) enact as home grounds for natural biodiversity and lift the efficiency to maintain nutrient and microbial levels within the water column. On the other hand, onshore aquaculture systems provide a better possibility for environmental control, biosecurity measures, and a smaller environmental footprint in comparison with open systems. Besides, sustainable management on the pressing environmental sanitation issues (pollution and effluent discharge) needs to be given special attention in those areas where petite or sparse freshwater regulatory measures exist75.

In order to ensure food safety and thereby preventing food-borne illnesses, rapid and reliable detection of pathogens and/or toxins is required. The farm managers, food producers, processors, distributors, handlers, and vendors bear the primary responsibility, whereas the consumers shall remain attentive. The governing agencies must enforce and implement pragmatic food safety regulations to safeguard public health. Medical practitioners need to remain enthusiastic to prevent such illnesses and treat those diseases with a safe diet under proper supervision. Veterinarians, aquaculturists, and agriculturists shall shoulder collaboration with all their stakeholders in the light of chemical and pathogen spillover with an ultimate aim to ensure food safety in the larger interest of the society.