Perspective Chapter: Health and Safety in Oyster Aquaculture

Abstract

The globalization of oyster markets has accelerated the commercial exchange of food, needing to implement strategies that contribute to ensuring the safety of food products. Among the factors that can threaten the safety of oysters are chemical contaminants (heavy metals, antibiotics, pesticides, etc.), biological (viruses, bacteria, etc.), and physical (pieces of metal, splinters, among others). These characteristics, together with the organoleptic, commercial, and nutritional ones, constitute the basic requirements that must be considered to access the various markets because they provide a high degree of confidence to the consumer. Oyster products for human consumption need a sanitary certification that guarantees the quality of their products and ensures competitive and permanent participation in the market. To achieve this, each link in the chain food industry must establish controls and activities that minimize contamination risks.

1. Introduction

Oysters are one of the best known and most widely cultivated marine animals, which are highly valorized seafood products, and a large part of the international seafood trade recognized for their crucial role in food security and nutrition as a source of basic nutrients such as proteins, essential fats, minerals, and vitamins. Commonly farmed food oysters include the Eastern oyster (Crassostrea virginica), the Pacific oyster (Crassostrea gigas), Kumamoto oyster (Crassostrea sesame), Chilean flat oyster (Ostrea chilensis), Belon oyster (Ostrea edulis), the Sydney rock oyster (Saccostrea glomerata), Olympia oyster (Ostrea lurid), and the Southern mud oyster (Ostrea angasi) [1]. Oyster mariculture is achieving spectacular development worldwide, constituting a growing food sector with economic development opportunities for the coastal economy. World production of oysters stands out with more than 4.5 million tons, producing a yield of approximately 3.7 billion dollars, with C. gigas being the most widely cultured species. Prioritizing and better integrating aquaculture products in global, regional, and national food system strategies and policies should be a vital part of the necessary transformation of the agrifood systems. This trend has to be maintained or increased to maintain the current levels of consumption of oyster products as the world population continues its increase [1, 2].

The globalization of oyster markets has accelerated the commercial exchange of food, increasing the problems related to food biosecurity, with the necessity to implement strategies that contribute to ensuring the safety of food products. Aquaculture products typically pose a health risk to consumers through contamination from the environment, in which they are grown, their inherent chemical composition, cross-contamination during handling, improper processing, poor storage, distribution practices, and marketing [3]. Particular hazards are associated with the consumption of oyster products, usually defined as the physical, chemical, or biological agents present in the food or one of its properties, which can cause harm to the health of the consumer when being ingested. Expanding the trading of oyster products requires scaling up transformative changes in policy, management, innovation, and investment to achieve sustainable, inclusive, and equitable global aquaculture with inherent food biosecurity [2].

2. Food safety risks of oysters

Oyster aquaculture has long been an important food source and livelihood for millions worldwide, consumed by inhabitants of all five continents. However, if oyster food products are not handled, stored, and processed correctly, their safety may be affected due to contamination by different agents. Hazards can occur at various stages of the production chain and vary depending on the aquatic environment from which they come and postharvest handling and processing procedures. Identifying the hazards associated with aquaculture products is essential to understanding the level of risk in food safety. Investigations of disease outbreaks linked to oyster consumption have been reported in the scientific literature; however, only a few countries systematically collate and report such data through a disease surveillance system [3]. Oysters are filter feeders, so they naturally concentrate anything in the surrounding water. Oysters can be contaminated with biological (viruses, bacteria, parasites), chemicals (e.g., heavy metals, marine biotoxins), and physical agents (e.g., glass and metal fragments) [4].

2.1 Biological contamination

Oysters and many commercial bivalve species are prevalent in coastal estuaries, as well as similar shallow or drying areas, where nutrient levels are high, and the waters are sheltered. Unfortunately, such shallow, in-shore, growing waters are frequently contaminated with human and animal sewage. In the process of filter-feeding, bivalve shellfish may also concentrate and retain human pathogens derived from such sewage contamination and naturally occurring marine pathogens [5]. Biological contamination refers to microorganisms that can potentially contaminate food and harm consumers’ health. These biological hazards include parasites, viruses, and pathogenic bacteria [6].

Oysters are known as a potential source of protozoan parasites such as Toxoplasma gondii (responsible for toxoplasmosis), Cryptosporidium spp. (one of the major causes of gastroenteritis in the world), and Giardia spp. (responsible for gastroenteritis) [7, 8, 9, 10, 11, 12]. Crassostrea belcheri oysters can be an effective transmission vehicle for Cryptosporidium parvum oocytes, especially within 24–72 h of contamination, with viable oocysts present at up to 7 days postinfection. Unless consuming well-cooked oyster dishes, eating raw oysters remains a public health concern, and in general, at least 3 days of depuration in clean sea water before consumption is recommended [12]. Many reports have shown that Toxoplasma gondii is present in C. virginica and other Crassostrea species, being potential sources of contamination for humans and other animals [7, 13, 14]. Although T. gondii infections are largely asymptomatic or clinically mild in immunocompetent individuals, infection in immunocompromised patients and fetuses infected congenitally may lead to serious health consequences [15, 16]. Cryptosporidium and Giardia were detected in commercial and noncommercial oysters (C. gigas) and water from the Oosterschelde, the Netherlands, suggesting that consuming raw oysters may occasionally lead to cases of gastrointestinal illness [11].

Among metazoo parasites of oysters are trematodes and nematodes with zoonosis impact [17]. Foodborne illnesses appear when raw or undercooked fish products containing the parasite in its infective stage are consumed [3]. Most of these diseases are rare and cause only mild or moderate damage, but some pose serious health risks. Some metacercariae of the families Echinostomatidae (they encyst in various tissues) and Gymnophallidae (they occur without encysting between the mantle and the valve, erecting very varied responses that compromise the mantle and the valve) are of public health importance as they are potential parasites of human [18]. In Korea, an endemic zoonosis is caused by consuming raw oyster C. gigas, parasitized by Gymnophallidae metacercaria [19]. Recently Grano-Maldonado et al. [20] and Tejeda-Arenas et al. [21] reported the first incidence of the digenean Stephanostomum sp. (Acanthocolpidae), encapsulated and embedded in the digestive gland and mantle tissue, parasitizing Crassostrea corteziensis on Mexican coasts, and other digeneos (Families Hemiuridae, Fellodistomidae, and Zoogonidae) with possible implications for the health risks posed by human consumption. Although nematodes are uncommon as bivalve parasites, few Ascaridoidea and Spirurida Nematoda species could be found as larval stages without specificity for their site infection. Indeed, they frequently appear in low prevalences and infection intensities, eliciting different capsules. Some ascaridoids are potentially pathogenic to human health [17, 22]. Second and third instar larvae of Echinocephalus crassostreai occur in C. gigas from culture off the coast of Hong Kong and adjacent coasts of China [23]. Humans ingesting this nematode can cause granulomatous gastric lesions [22, 24].

Foodborne viruses are an important and emerging problem for food safety and public health, according to a report by EFSA [25]. Oysters, aquatic filter feeders, are a notorious source of foodborne viral infections because they actively concentrate viruses from contaminated water [5, 26]. Some viruses have been epidemiologically linked to disease following the consumption of oysters or other bivalves transmitted by the fecal-oral route, many of which can contaminate oyster or their harvesting areas. Illness has been related to viruses causing gastroenteritis and viruses causing hepatitis [5, 27]. In situ studies with bioaccumulation of a virus indicator in oysters have shown that oysters can concentrate viruses up to 99 times compared to the surrounding water [28]. Oysters are often eaten raw, creating the potential for foodborne enteric virus infections. The leading cause of viral diseases transmitted by consuming raw or undercooked oysters (although some outbreaks have been linked to cooked oysters) is enteric viruses from infected people and animals, either via infected handlers or by contamination of the aquatic environment with the excrement of humans or animals [29]. The pathogens most frequently involved in these outbreaks are noroviruses (NoVs; responsible for acute gastroenteritis in humans, which is particularly hazardous for immunocompromised or chronically ill persons), and adenoviruses (AdVs, often linked with respiratory illness, gastroenteritis, and neurological diseases) [3, 30, 31, 32, 33]. Norovirus has been detected in 5 to 55% of oysters from Europe, the United States (US), and Brazil by random sampling at marketplaces, oyster farms, and environmental samples [34, 35, 36, 37], and in 2010, NoVs outbreaks were linked to oyster consumption in the United Kingdom, Norway, France, Sweden, and Denmark [38, 39]. Ng et al. [40] reported associated outbreaks of norovirus gastroenteritis in Singapore. Le Guyader et al. [31] reported multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption. Internationally distributed frozen oyster meat caused numerous outbreaks of norovirus infection in Australia [41]. In December 2009, over 200 individuals reported gastrointestinal symptoms associated with oyster consumption after dining at a North Carolina restaurant [29]. Noroviruses are difficult to remove from oysters through cleansing and also stay infectious even if cleaned [42]. A difference in accumulation and persistence between different strains of NoV in a single species of shellfish has been shown [32, 43] such as the oyster Crassostrea ariakensis that was shown to more efficiently accumulate NoV, murine norovirus 1, and hepatitis A virus than C. virginica [44]. Two New Zealand outbreaks of norovirus gastroenteritis linked to commercially farmed oysters were reported [45]. Multiple NoV genotypes have been characterized by an oyster-associated outbreak of gastroenteritis [46]. In Taiwan, surveillance of AdVs and NoVs contaminants in the water and shellfish of major oyster breeding farms was reported [33]. Moreover, AdVs can persist in the environment for a longer time and are considered one of the potential human viral indicators present in fecal-contaminated waters [47].

A wide range of positivity rates for rotavirus A (RVA) has been reported in oysters from different regions from 3.3% to 57.8% in Thailand, Japan, France, Mexico, and Argentina [37, 48, 49, 50, 51, 52, 53]. Rotaviruses are the most important pathogens responsible for diarrheal deaths in children under 5 years of age, with more than 128,000 deaths worldwide each year [54, 55]. In addition, rotavirus was detected in 0.3–16.7% of cases with oyster-associated gastroenteritis [27, 51]. Oyster has been considered an important carrier of RVA transmission [27, 56]. Rotavirus has been detected in farmed oysters at rates of 3.3–44.4% [51].

Hepatitis A (HAV) is the most severe virus infection linked to shellfish consumption, causing serious debilitating disease and even, occasionally, death. Any man may contract HAV after consumption of contaminated shellfish that has not been thoroughly cooked, and many HAV outbreaks worldwide have been linked to bivalve mollusk consumption and have been reviewed by several authors [5, 57, 58, 59]. The first documented shellfish-borne outbreak of “infectious hepatitis” occurred in Sweden in 1955 when 629 cases were associated with raw oyster consumption [60]. Large outbreaks of infection involving >800 patients also occurred in Australia in 1979 [61], the United States in 1986 [62], and Japan in 1991 [63]. Conaty et al. [64] reported hepatitis A in New South Wales, Australia, from the consumption of oysters. The ability of HAV to persist was demonstrated for up to 6 weeks in Eastern oysters (C. virginica). These results support that oyster depuration is insufficient for completely removing infectious viruses. Extended relay times (more than 4 weeks) may be required to produce virologically safe shellfish [65]. C. ariakensis efficiently accumulated HAV [44]. In France in 2007, 111 HAV cases linked to the consumption of raw shellfish (mainly oysters) were present in one French farm and the surrounding area [66]. Also, in the United States (2005), 39 HAV cases were epidemiologically linked to consuming raw oysters from two Louisiana harvest areas [67, 68]. HAV can persist for several weeks in oysters despite depuration techniques. This virus is also fairly resistant to heating and may remain viable in shellfish after up to 5 minutes of steaming [69]. Shellfish-associated HAV outbreaks occur globally and are likely underreported. The relatively long incubation period from the time of exposure to the onset of symptoms renders tracing and detection of a common source difficult.

Also, oysters may be vectors of hepatitis E (HEV). Infected individuals excrete HEV, which is present in wastewater and coastal waters. HEV shares morphological and biophysical characteristics with caliciviruses; however, there are significant genomic differences. Recent taxonomic proposals leave HEV without a formally assigned virus group [70]. HEV is generally mild but can be more severe for pregnant women. Song et al. [71] described the first report of the detection in oysters of HEV that may have originated from genotype 3 swine HEV in Korea. They showed a close genetic relationship with the swKOR-1 strain and the swine and human HEV isolated in the USA. Grodzki et al. [72] demonstrated that oysters might accumulate HEV experimentally in C. gigas and O. edulis; tissue distribution analysis showed that most of the viruses were concentrated in the digestive tissues. Also, they collected 286 samples, and none were contaminated with the HEV virus despite evidence that this virus is circulating in some French areas. The number of HEV viral particles discharged into the environment is too low to detect, or the virus may persist very short in pig manure and human waste. However, as shellfish is a typical food in France, this transmission route cannot be excluded from consideration, although shellfish have not yet been implicated in an HEV outbreak in France.

Oysters can also contain harmful bacteria. Vibriosis is an illness caused by some kinds of Vibrio bacteria when eating raw or undercooked oysters. Vibrio naturally lives in coastal water, and the oyster that contains The Vibrio bacteria does not make an oyster look, smell, or taste any different, which makes it hard to detect. Cooking oysters properly can kill Vibrio and other harmful germs they might contain. Most Vibrio infections from oysters result in mild illness, including diarrhea and vomiting. However, people with a Vibrio vulnificus infection can get very sick. Infections caused by ingesting V. vulnificus can result in gastroenteritis with associated abdominal pain, diarrhea, and vomiting but have the potential to quickly progress to primary septicemia, exhibiting blistering skin lesions or organ failure, with mortality rates for sepsis and wound infection. V. vulnificus is the most deadly seafood-borne pathogen [73, 74, 75]. Also, infection with Vibrio cholerae is very serious and debilitating [76]. Cholera outbreaks can be initiated by transmission of “epidemic” or “non-epidemic” V. cholerae strains from their environmental reservoir to humans through seafood or other environmentally related food or water sources [77]. “Epidemic” strains of V. cholerae carrying a suite of specific virulence genes cause the disease cholera, characterized by the rapid onset of profuse, watery diarrhea, which, if untreated, can lead to dehydration, circulatory collapse, and death. V. cholerae strains belonging to serogroup O1 were believed to be the sole etiologic agents of cholera, and the signs and symptoms of cholera are caused by cholera toxin. Strains of V. cholerae that do not carry the virulence factors necessary to cause epidemic cholera have been implicated as causes of diarrheal disease, wound infections, and, in susceptible hosts, septicemia [76, 77]). Epidemiologic studies and studies involving volunteers have linked the occurrence of diarrheal illness to the production of a heat-stable enterotoxin (NAG-ST) similar to that produced by enterotoxigenic Escherichia coli [77]. Other species are associated with gastroenteritis of varying severity, including Vibrio parahaemolyticus infection, which is quite commonly associated with eating undercooked oysters. Still, most cases are sporadic because not all strains of V. parahaemolyticus are considered pathogenic. The thermostable direct hemolysin (encoded by tdh), which is the virulence factor associated with pathogenic functions in humans and marine animals, is rare to occur in marine environmental V. parahaemolyticus bacteria [78, 79, 80], although pathogenic serotypes have been found in raw oysters [80, 81]. The most common clinical presentation is watery diarrhea, but other symptoms include abdominal cramps, nausea, vomiting, headache, fever, and bloody diarrhea. Sepsis due to V. parahaemolyticus is quite rare and occurs primarily in patients with cirrhosis and neutropenia [76, 77]. Also, V. mimucus was reported acute gastroenteritis in patients who had recently ingested raw oysters [82], and Vibrio hollisae has been recovered from patients with gastroenteritis who consumed raw seafood before their enteric illness [83].

Other bacteria, such as Campylobacter spp., Salmonella spp., Shigella spp., Plesiomonas shigelloides, Clostridium spp., and E. coli, which are commonly implicated in gastroenteritis, are only occasionally traced to seafood [76, 84]. The vast majority of Salmonella isolates from oysters in the United States were Salmonella enterica serovar Newport, a major human pathogen, confirming the human health hazard of raw oyster consumption [85, 86], and is capable of surviving within oysters for at least 2 months within a laboratory setting [87]. Shellfish are frequently contaminated by Campylobacter spp. presumably originating from feces from gulls feeding in the growing or relaying waters [88]. Oysters have been shown to harbor species of Campylobacter (primarily C. lari, but also C. jejuni, C. coli, and C. upsaliensis), a source for human infections [89, 90]. Symptoms can range from mild to serious infections in children and the elderly and permanent neurological symptoms [91]. Sharp [92] reported a case of a prosthetic hip infection caused by C. coli by ingesting contaminated raw oysters. Also, Shigella has been responsible for many seafood-associated outbreaks, mainly from consuming raw oysters. Shigellosis symptoms include diarrhea, which can be watery, bloody, and/or contain mucus or pus, stomach pain and cramps, vomiting, fever, and complications, are rare but include seizures in young children, toxic megacolon, bacteremia, Reiter’s syndrome, and hemolytic-uremic syndrome [84, 93, 94]. Also, Clostridium species have been reported in oysters, in untreated (influent) and treated (effluent) wastewaters, and in harvest waters [95]. Toxin-producing C. difficile causes a wide range of clinical manifestations in the host from asymptomatic colonization to diarrhea and even death [96]. Moreover, E. coli occurrence in seafood is considered a sanitary case and may represent a risk to the consumers if related to diarrheagenic E. coli. This bacterium in seafood is related to water contamination and/or unhygienic conditions during the handling process, being the potential cause of the quality of the ice used for conservation and the food processing plants. However, the presence of non-pathogenic E. coli in fish and shellfish should also alert public health since enumeration of E. coli is the standard way to assess the level of fecal microorganisms in water and shellfish and indirectly to estimate the associated potential risk to human health from all waterborne enteric pathogens [97].

2.2 Chemical contamination

Microorganisms are not the only cause of foodborne illness. Oysters that thrive in coastal areas, estuaries, or bays may be exposed to environmental contaminants from various sources such as rivers, marine currents, urban discharges, and natural phenomena. Biotoxins and chemical compounds, such as pesticides, organochlorines, organophosphates, heavy metals, and veterinary drugs, can be incorporated and accumulated into these organisms and cause public health problems [6, 98]. The risk of acute poisoning is very low; however, long-term exposure to high levels of chemical contaminants in food may be associated with severe diseases such as neurological damage, birth defects, cancer, and death [99, 100].

Marine biotoxins are often associated with harmful algal blooms when toxins accumulate in oysters and other shellfish and cause human disease. Shellfish poisoning human syndromes are classified as diarrhetic, amnesic, neurotoxic, paralytic, and azaspiracid [101]. Most of these toxins are produced by species of naturally occurring marine algae (phytoplankton). There are approximately 5000 species of marine algae, but only 70–80 species are known to produce toxins. During filter feeding, these organisms are bioaccumulated by oysters and other shellfish and then release their toxins into their tissues. In most cases, a complex suite of toxins can be produced by a given phytoplankton species, and these can be further metabolized by the shellfish, producing, in some cases, more potent derivatives of the precursor molecules [102]. Outbreaks of intoxication in humans due to marine biotoxins are caused by ingesting contaminated shellfish and can have a wide range of symptoms linked to the specific toxic compound [103, 104]. These marine biotoxins can cause massive economic losses to the aquaculture industry due to the cautionary closure of cultivation areas [105].

Diarrhetic shellfish poisoning (DSP) is a seafood intoxication that consists of rapid-onset gastrointestinal symptoms, such as vomiting and diarrhea. Recovery usually occurs within 3 days, with or without medical treatment. The diarrhetic shellfish toxins are polyether compounds and are grouped into four structural classes: okadaic acid (OA) and its derivatives (dinophysistoxin or DTX), pectenotoxin (PTX), yessotoxin and its derivatives (YTX), and azaspiracid (AZA) [106]. The symptoms caused by the OA group, produced by dinoflagellates of the genera Dinophysis and Prorocentrum, include diarrhea, nausea, vomiting, and abdominal pain, starting 30 min to a few hours after consumption of contaminated shellfish, with complete recovery within 3 days [107]. Chronic exposure to OA, such as polyether toxins, has been identified as a tumor promoter [108, 109]. Among the other mentioned classes, PTX and YTX have not been implicated in human illness. AZAs produce a severe toxicity syndrome in humans, causing mainly gastrointestinal problems, such as cramps, vomiting, nausea, and severe diarrhea [110]. Members of the marine dinoflagellate family Amphidomataceae, including the genera Azadinium and Amphidoma [105, 111], have been recognized as producers of a unique group of lipophilic polyether phycotoxins known as azaspiracids (AZAs). Among species of Azadinium and Amphidoma languida, more than 30 AZA analogs have been described [112]. The first incidence of human shellfish-related illness identified as DSP occurred in Japan in the late 1970s; the dinoflagellate Dinophysis fortii was identified as the causative organism; the toxin responsible was termed dinophysistoxin (DTX-1) [113, 114]. Many outbreaks of the diarrheic toxins worldwide have been reported in commercial harvest oyster areas [105, 115, 116, 117, 118].

Amnesic shellfish poisoning (ASP) is caused by the consumption of shellfish that have accumulated domoic acid (DA), a neurotoxic amino acid belonging to the kainoid class of compounds, produced by some strains of microalgae, such as the diatom Pseudo-nitzschia [119]. The clinical effects observed in many of the affected individuals included memory loss, and for this reason, the condition was termed amnesic shellfish poisoning (ASP). The neurotoxic properties of DA by oral exposure to a few mg/kg result in neuronal degeneration, necrosis in specific regions of the hippocampus, and gastrointestinal effects, while slightly higher doses cause neurological symptoms, seizures, memory impairment, limbic system degeneration, and coma [120, 121]. Domoic acid and its isomers are water-soluble and do not degrade under ambient temperatures or when exposed to light in a sterile saline solution [122]. However, it has been shown to decompose under acidic conditions (50% DA loss in 1 week at pH 3) [123]. A serious outbreak of ASP occurred in Canada in 1987 and involved 150 reported cases, 19 hospitalizations, and four deaths after consuming contaminated mussels [121]. However, there are geographical, temporal, and species variations of DA in bivalve mollusks, as observed in organisms sampled in cultivated areas of Ireland, where the toxin was found predominantly in the hepatopancreas of scallops (Pecten maximus), and only trace levels of DA were present in mussels (Mytilus edulis) and oysters (C. gigas) [124].

Neurotoxic shellfish poisoning (NSP) is a disease caused by the consumption of molluscan shellfish contaminated with brevetoxins (PbTx); a suite of nine structurally related ladder-like polycyclic ether neurotoxins produced by the marine dinoflagellate, Karenia brevis [125]. Brevetoxins comprise a group of toxins with primarily neurological and gastrointestinal effects. Rinsing, cleaning, cooking, and freezing do not destroy the toxins, which cannot be detected by taste or smell. Symptoms of NSP include nausea, vomiting, diarrhea, paresthesia, tingling, numbness of the perioral area, loss of motor control, severe muscular ache, cramps, bronchoconstriction, seizures, coma, and, in extreme cases, may lead to death [126, 127]. NSP has been reported in temperate areas worldwide, including the southeastern coast of the United States, the Gulf of Mexico, the Caribbean, and New Zealand. Oysters and other bivalves were implicated in the major outbreak of NSP in New Zealand in 1992–1993, with over 180 cases reported over several weeks. A review of this outbreak involved Karenia mikimotoi as the likely causative agent, but other suspect species were also present in the bloom. Although PbTx was implicated, more than one group of marine toxins and more than one algal species appear to have been involved [127]. The largest reported outbreak of NSP in the US occurred in North Carolina after K. brevis was carried into that region. Illness was observed in a few cases where less than 12 oysters were consumed, but the attack rate was 65% among those eating 12 oysters or more [126, 128, 129].

Paralyzing shellfish poisoning (PSP) is caused by the consumption of shellfish contaminated with highly potent neurotoxins, saxitoxin (STX), and its analogs, produced by certain species of harmful algae such as microalgae of the genera Alexandrium, Gymnodinium, and Pyrodinium [130, 131] and some freshwater cyanobacteria [132]. The earliest documented report of intoxication by PSP toxins occurred in Canada in 1798 [131]. Symptoms of PSP include paresthesia and numbness, first around the lips and mouth and then the face and neck, muscular weakness, a sensation of lightness and floating, ataxia, impaired motor coordination, drowsiness, incoherence, and progressively decreasing ventilator efficiency. In severe cases, toxicity results in paralysis and death. Usually, death occurs within 1–12 h post-exposure [133]. Suffocation with cardiac arrest is the common reason for death. Acute toxicity of PSP toxins exposure is well known; however, chronic deleterious effects still need to be elucidated. PSP toxins are heat stable and are not destroyed by standard cooking procedures, marinating, or freezing. Cooking can increase toxicity by converting the less toxic derivatives into more toxic forms. Thus, it is crucial to monitor and control this hazard in the growing shellfish areas [102]. The first case of PSP was recorded in 1927 near San Francisco, United States, and was caused by Alexandrium catenella, resulting in 106 human illnesses and six deaths [134]. The Philippines has the highest number of PSP cases reported in Asia [135], with 2124 PSP cases and 120 deaths reported from 1983 to 2002. Around 2000 human PSP cases are reported worldwide annually, with 15% fatalities [136].

Using pesticides and other chemicals in agriculture produces environmental risks through biomagnification in trophic nets and bioaccumulation in organisms destined for human consumption. Pesticides, such as organochlorines, organophosphates, and heavy metals, have relative importance since they can be captured and accumulated by oysters and another bivalve mollusk during the leak process and cause any harmful effect to the consumer if the former is not subject to an efficient purification process. Due to their physiological characteristics, bivalve mollusks possess the capacity to bioaccumulate concentrations of contaminants that exceed levels present in the surrounding environment, thus making it possible to detect even trace levels of toxic substances [98]. In farmed C. gigas on the Mexican coast detected, organochlorine pesticides (endosulfan, DDE, lindane) and metals (Zn, Cd, and Pb) [137]. These organochlorine pesticides are all listed among the most dangerous toxic compounds established by the Stockholm Convention in 2013. Concentrations of lipophilic organic compounds, such as DDT, in the oyster C. virginica increase at sexual maturity when oysters produce lipid-rich gametes [138]. Oysters also eliminate these pollutants through spawning (release of eggs into the water). With C. virginica, the risk to humans is, therefore, most significant at the moment of sexual maturity. Studies demonstrated that endosulfan and its metabolites possess a carcinogenic potential and produce mutagenic and genotoxic effects in human lymphocytes and liver hepatoblastoma cells [139, 140, 141]. DDE’s impact on humans includes cancer development, primarily in women [142], and lindane is a possible human carcinogen. Deltamethrin (DEL), an insecticide belonging to the pyrethroid family, became the preferred choice in many agriculture-based countries in the last two decades since the implementation of restrictions on the sale of organophosphorus insecticides can be introduced into the food chain through bioaccumulation in C. gigas and then potentially threatens human health [143, 144].

Estuarine and coastal ecosystems are often considered vulnerable due to the complex biogeochemical processes and human disturbances through a variety of pollution. Among environmental contaminants, heavy metals in estuarine and coastal ecosystems have been of increasing concern in environmental conservation. Oysters can also be contaminated by heavy metals, which can be carried through the water of the rivers and enter the first link of the trophic chain (microalgae) to later pass to mollusks or be absorbed directly from the water column. Acute toxicity resulting from consuming contaminated food is uncommon, but chronic exposure can result in undesirable toxic effects and symptoms of heavy metal poisoning can be life-threatening, and they can cause irreversible damage. Toxicity from heavy metals depends on the type of metals and the amount taken. Some heavy metals, including arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb), and mercury (Hg), are harmful to humans, even at trace concentrations [145]. Oyster and 16 seawater samples collected from the southern coast of Korea, including designated shellfish growing areas for export, showed the metal bioaccumulation ratio in oysters that was relatively high for Zn and Cd but low for Hg, Pb, As, and Cr [146]. In various oyster species, mobile cells called amebocytes accumulate complex metals in the blood. In O. edulis and C. virginica, some amebocytes accumulate copper (Cu), others Zn, or Cu and Zn simultaneously [147]. Other oyster species, such as Ostrea angasi and C. gigas, have only one amebocyte type, which accumulates Cu and Zn equally well [148, 149]. Such species may accumulate high levels of contaminants in some of their tissues. When these species are consumed, the metal-metallothionein complexes, enzymes of the oysters, which form complexes with the trace elements and render them harmless, are ingested and digested, releasing the metals into the consumer’s body in a manner that favors the assimilation of the metals. Therefore, the levels transferred to and absorbed by the consumer may be high [150]. Long-term exposure to inorganic Ar evidence is strongest for high blood pressure, heart attacks, circulatory disease, producing tingling and loss of sensation in the limbs, and causing brain damage. Pb is a toxic heavy metal even at very low levels of exposure in humans and targets multiple organs in the body due to its systemic toxicity, which can cause neurological, cardiovascular, renal, gastrointestinal, hematological, and reproductive effects. Cd produces kidney and bone damage, and it does not degrade in the environment to less toxic products, contributing to its bioaccumulation in the kidneys and liver. Moreover, Cu can damage the liver and kidneys, and metals, such as chromium (Cr) and nickel (Ni), have been linked with cancers [151].

Moreover, pharmaceutical residues, dioxins, polycyclic aromatic hydrocarbons (PHAs), and polychlorinated biphenyls (PCBs) have been found in the marine environment, so they also could qualify as pollutants of interest in oysters [152, 153, 154, 155, 156]. The inappropriate use of antibiotics can harm human health by making it difficult to treat diseases due to antimicrobial resistance. Furthermore, residues present in shellfish can make the product unacceptable to consumers [98]. Chloramphenicol, the most widely used antibiotic in bivalve hatcheries, has a long half-life, is highly toxic, and can cause larval deformities and known risks to humans, in addition to favoring the development of resistance [157]. Dioxins, PAHs, PCBs, and other organic compounds are very chemically stable molecules and, therefore, difficult to destroy. They remain in the ecosystem for years; some accumulate in the trophic chain. These compounds reach the marine environment through different sources: wastewater and industrial effluents, land runoff, or atmosphere deposition. Dioxins are primarily by-products of industrial processes but can also be produced in natural processes, such as volcanic eruptions and forest fires. They can accumulate in oysters affecting egg fertilization and development [158]. Dioxins are highly toxic to humans and can cause reproductive and developmental problems, affect the immune system, interfere with hormones, and thus cause cancer [159]. Also, there are concerns over health risks due to their accumulation of PAHs, which are organic contaminants exhibiting carcinogenic toxicity [160, 161, 162]. They originated during the incomplete combustion or pyrolysis of organic material, such as coal, oil, and gasoline, open dumps, forest fire, and in coastal marine sediments due to petroleum products deliveries and fuel combustion emissions from the ships staying alongside the quays [163, 164]. Oysters tend to concentrate very high levels of PAHs, and the lipophilicity of the organic compounds affects the accumulation patterns [154]. PCBs release into the environment through spills, leaks from electrical and other equipment, and improper disposal and storage and have been detected in the whole soft tissue of oysters [153]. A high concentration of PCBs is associated with neuropsychological and neurobehavioral deficits, dementia, immune system dysfunctions, cardiovascular diseases, and cancer and can reduce fertility [165].

2.3 Physical contamination

Physical hazards in animal feed and feed ingredients are mainly foreign objects in the food that make it unsafe for consumption since they can cause suffocation or injuries to the hands, mouth, and gastrointestinal tract. These hazards are recognized mainly by consumers and commonly reported by consumers. The typical physical hazards associated with aquaculture and fishery products are glass pieces, wood splinters, thorns, stones, hooks, and metal fragments [6, 100]. Some can be found in these products, such as hooks after their capture or harvest; others may come from the facilities, equipment, and utensils, where they are processed [3]. The Food and Drug Administration (FDA) Health Hazard Evaluation Board considers that foreign objects with dimensions less than 7 mm rarely cause severe trauma to consumers, except in risk groups, such as infants and the elderly [100, 166]. In oysters, it is common the presence of hard or sharp parts, such as shells, becomes hazardous if consumers do not expect them. The recent problem in marine edible species is the presence of microplastics [167, 168]. A systematic review shows that 94.4% of all oysters globally had microplastics, with an average of 1.41 ± 0.33 per gram of soft tissue wet weight. The study showed that wild-caught oysters contained more than double the amount of microplastic than aquaculture-raised specimens. Polymer type in commercially farmed oysters (C. gigas and Saccostrea glomerata) across a broad spatial scale, covering eight sites in southern Australia, identified that 62% of the verified microplastics were vexar plastic netting, a low-density polyethylene commonly used in aquaculture production [169].

2.4 Spoiled oyster

Despite significant progress in processing, refrigeration, and transportation, millions of tons of aquatic products are lost or nutritionally compromised yearly. Seafood commodities are among the most perishable foods and rapidly produce numerous compounds associated with objectionable odors. Oysters can have a reasonably long shelf life of up to four weeks, but their taste becomes less pleasant as they age. Preferably oysters must be eaten, cooked, or processed alive; however, oysters can be eaten on the half shell, raw, smoked, boiled, baked, fried, roasted, stewed, canned, pickled, steamed, broiled, or used in various drinks. If not correctly treated after harvesting, they can soon become unfit to consume and possibly dangerous to health due to microbial growth, chemical change, breakdown by endogenous enzymes, and cross-contamination leading to food safety risks. Proper handling, processing, preservation, packaging, and storage measures are essential to extend shelf life, ensure food safety, maintain quality and nutritional attributes, and avoid loss and waste [2].

After shellfish harvest, food-handling precautions should be followed to avoid the introduction of foodborne pathogens, as would be appropriate for any raw or processed food. Proper workers’ hygiene, gloves, and regular hand washing must be practiced. The deterioration of oysters is mainly attributed to the combined activities of microbiological metabolism and biochemical deteriorations, such as enzymatic decomposition and PUFA oxidation [170, 171]. The freshness of oysters is a function of bacterial activity, which directly affects flavor, odor, texture, and color. One technique used to assess the bacterial quality of oysters is the aerobic plate count (APC), which determines the number of total aerobic microbes from which individual isolates may be further identified [172]. Changes in the microbial flora of C. gigas during refrigerated storage showed that Vibrionaceae and Pseudomonas were predominant in freshly harvested and shucked oysters. In contrast, Pseudomonas bacteria increased dramatically after 12 days of refrigerated storage, while Vibrionaceae remained at the same level [173]. Total bacteria above 107 cfu⁻¹ is not considered acceptable quality [174]. Cao et al. [173] also found other spoilage-associated bacteria, accounting for lower proportions and decreases during storage, such as the H2S-producing Shewanella putrefaciens, and gram-negative bacteria Enterobacteriaceae, Moraxella, and Flavobacterium. Fernandez-Piquer et al. [175] evaluated the effect of postharvest temperature on bacterial communities in live C. gigas using nonculture-based methods and found that members of the Proteobacteria predominated before storage, while storage altered the bacterial profile with Psychrilyobacter spp. predominated at 4°C, while at 15 and 30°C, members of the phylum Bacteroidetes represented the highest percentage. Microbial diversity in oysters was observed, with at least 73 different genera-related clones among all samples, using microbial culture and pyrosequencing 16S rRNA.

Temperatures of 7, 13, and 21°C, during raw C. virginica harvesting and storage, may allow for the multiplication of natural spoilage flora, as well as microbial pathogens such as V. vulnificus, thus posing a potential health threat to susceptible consumers and compromising product quality [176]. Moreover, the concentrations of microbiological groups of organisms increased with the duration and temperature of storage and were higher in fully processed oysters than in shucked meats. Total counts of bacteria, fungi, coliforms, fecal streptococci, Aeromonas hydrophila, and Clostridia were significantly higher in shucked oysters than in those stored as shellstock [177]. The bacterial spoilage of C. gigas and Saccostrea glomerata, during storage at 4°C, revealed that the majority of bacteria at day 0 represented taxa from among the Proteobacteria, Tenericutes, and Spirochaetes, while during storage, Proteobacteria became abundant with Pseudoalteromonas and Vibrio found to be dominant in both oyster species at day 7 [171]. Bacterial spoilage profiles in the gills of C. gigas and C. virginica during refrigerated storage at 4°C showed that Psychrobacter and Psychromonas (psychrotrophic genus) were represented as the most important gill spoiled bacteria, and Arcobacter with pathogenic potential was the dominated bacteria in all spoiled oysters [178]. Also, as oysters spoil, a slight but important reduction in pH is noted. Fresh oysters have a pH of about 6.3, but when spoiled have a pH of six or less [173, 176], although Madigan et al. [171] and Chen et al. [178] found that pH increased with the prolonged storage time and spoiled. Although shellfish may remain viable in cold storage for a couple of weeks, it is clear that spoilage can begin within 1–2 weeks. Therefore, after more than 2 weeks, live shellfish may be unsafe to eat [179].

Interventions that reduce bacterial pathogens and non-pathogens (i.e., HPP and irradiation), to some degree, can inactivate spoilage bacteria, thereby somewhat extending the shelf life of shellstock and shucked shellfish [170, 180, 181, 182]. Cold storage of shellfish as shellstock rather than as shucked product may delay spoilage somewhat [177]. Data in C. gigas showed that chitosan treatment extended the shelf life of oysters from 8 to 9 days to 14–15 days [173]. The effect of super-chilling storage at −1°C depurated with ozone was studied in C. virginica, and without ozone in C. gigas, could better maintain the eating quality of shelled oysters and the extended shelf life to 9 and 21 days, respectively [183, 184].

3. Hazard analysis and risk assessment

Hazard analysis identifies all possible hazards potentially created by a product, process, or application. Risk assessment is the next step after the collection of potential hazards. Risk in this context is the probability and severity of the hazard becoming a reality. Among the factors that can threaten the safety of oysters and are considered hazards are biological and chemical contaminants and spoilage products, which have been recognized for many years. Consequentially, most countries have enacted sanitary controls on the production of oysters and other bivalve mollusks. These regulations cover similar ground on the requirements for clean growing areas, the management and processing requirements for more contaminated sites, the hygiene conditions for processing and dispatch establishments, requirements for marketing documentation, etc. [5].

To perform a hazard analysis as part of developing a plan, processors must have scientific information on potential hazards associated with raw materials and products for further processing [185]. It is important to consider naturally occurring food safety hazards in the environment from which oysters are harvested. Risks to consumer health from oysters caught in unpolluted marine environments are low, provided these products are handled according to good manufacturing practices. The risks of foodborne illness associated with aquaculture-derived oysters relate to inland and coastal ecosystems with a high potential for pollution. In some parts of the world, where shellfish are consumed either raw or partially cooked, there is an increased risk of foodborne parasitic, viral, or bacterial diseases. Health risks associated with chemical contaminants are difficult to assess because many produce long-term action (chronic risk), and evaluating the health impact of contaminated shellfish consumed by humans, exposure has to be estimated from contamination levels and consumption data. Also, as with all foods, some oyster health risks are associated with consuming certain products, which may increase when the catch is mishandled after harvest. Monitoring programs are in place in numerous countries worldwide, and oyster harvesting area closures occur when some contaminants are present.

The expansion in consumption and commercialization of aquaculture products has been accompanied by a significant development in food quality and safety standards. In this regard, FAO and the World Health Organization (WHO) are collaborating to identify and assess food safety hazards linked to the consumption of novel foods to provide the basis for further work for their control [186]. To meet these food safety and quality standards and ensure consumer protection, increasingly stringent hygiene and handling measures have been adopted at national, regional, and international levels, based on the Codex Code of Practice for Fish and Fishery Products [185], and the guidance it provides to countries on the practical aspects of implementing good hygiene practices and the hazard analysis and critical control point (HACCP)-based food safety management system [185, 187]. The Codex Alimentarius Commission was created in 1963 by the Food and Agriculture Organization of the United Nations (FAO) and World Health Organization (WHO) to develop food standards, guidelines, and related texts, such as codes of practice under the Joint FAO/WHO Food Standards Program. ​The Codex Alimentarius, “the food code,” plays a fundamental role in protecting consumers worldwide and ensuring fair practices in the food trade. The Code of Conduct for Fish and Fishery Products is the essential reference point for technical guidelines on the harvesting, processing, transporting, and selling of fishery products [185]. The main objectives of this program are to protect consumer health, ensure fair trade practices in the food trade, and promote coordination of all food standards work carried out by international governmental and nongovernmental organizations. The Codex Alimentarius demonstrates the potential hazards and defects that must be considered in aquaculture production. The code is intended to cover not only those safety hazards but also defect action points (DAPs), including the essential product quality, composition, and labeling provisions, and more, attempting to illustrate the potential hazards and defects at the various stages in the production chain.

One of the most important activities that must be performed in a processing facility as part of the food safety management system is determining if an identified hazard or defect is significant. The two primary factors determining whether a hazard or defect is significant for HACCP purposes are the probability of occurrence of an adverse health effect and the severity of the effect [185]. Carrying out a food risk assessment means estimating the probability and severity attributable to a given food hazard. This evaluation consists of five principal stages, which are resumed by Karunasagar [188]: (1) identify and characterize hazards: identification of biological or chemical agents capable of causing adverse health effects that may be present in a particular food or group of foods, with a qualitative or quantitative description of the severity and the duration of the adverse health effect that may result from the ingestion of the microorganism/toxin/chemical contaminants, (2) assess consumer exposure to such hazards: an estimate of the number of bacteria or the level of a biotoxin or chemical agent consumed through the concerned food is made, documenting the sources of contamination, frequency, concentration, and estimation of the probability and the concentration that will be consumed, (3) characterize the risks: the process of determining the qualitative and/or quantitative estimation, including attendant uncertainties of the probability of occurrence and the severity of the known or potential adverse health effect in a given population based on hazard identification, exposure assessment and hazard characterization, (4) management of risk: the process of weighing policy alternatives in the light of the results of risk assessment and if required, selecting and implementing appropriate control options including regulatory measures, and (5) risk communication: an interactive process of exchange of information and opinion on risk among risk assessors, risk managers and other interested parties (e.g., government agencies, industry representatives, the media, scientists, professional societies, consumer organizations, other public interest groups, and concerned individuals).

Once significant hazards and defects have been identified, consideration needs to be given to assessing their potential to be introduced or controlled at each process step. Control measures must be considered for significant hazard(s) or defect(s) associated with each step to eliminate possible occurrence or reduce it to an acceptable level. A hazard or defect may be controlled by multiple control measures [185]. For any given hazard or defect, it may be necessary to have more than one critical limit designated for each control measure. Critical limits should be established based on scientific evidence and validated by appropriate technical experts to ensure their effectiveness in controlling the hazard or defect to the determined level [185].

4. Aquatic health and biosecurity

The potential effects of harvesting and handling of products, onboard vessel handling, or in-plant production activities on the safety and suitability of oysters and their products should be considered at all times. In particular, this includes all points where contamination may exist and taking specific measures to ensure the production of a safe and wholesome product. The type of control and supervision needed will depend on the size of the operation and the nature of its activities.

As with many illnesses, prevention is the best medicine. Adequate cooking of oysters will kill the parasite and prevent infection. For those desiring raw or lightly steamed oysters, the risk of infection will still be present. Most edible bivalves, including oysters, are generally subject to purification or depuration, which places the shellfish in a clean water flow for 12 h or more. This enables the expulsion of many potentially harmful contaminants. Health certification of live oysters is now common as are monitoring and certification of grow out waters. However, depuration does not remove biotoxins produced by microalgae and other chemical compounds, and their control and impact on oyster production are generally managed by long-term monitoring programs. In severe contamination outbreaks, area closures may be necessary, and unless they can be reduced to an acceptable level by normal sorting and/or processing, no oysters should be accepted if they are known to contain parasites, undesirable microorganisms, pesticides, veterinary drugs or toxic, decomposed, or extraneous substances known to be harmful to human health. When oysters determined as unfit for human consumption are found, they should be removed and stored separately and either reworked or disposed of in a proper manner. All oysters deemed fit for human consumption should be handled properly, with particular attention being paid to time and temperature control [185].

It is generally accepted that the most effective and reliable approach to controlling the contamination of oysters is to harvest from areas with good water quality. Control of contamination through oyster processing procedures tends to be less effective, although providing a practical option for many countries, where waters may be subject to sewage contamination. Preharvest controls are the most effective means to address microbial and chemical hazards that are introduced via the seafood production environment. Monitoring programs vary according to hazard and the circumstances of their introduction. Monitoring approaches include measurements either from the water column directly or in the seafood species affected [102]. The current standards used to monitor the safety of shellfish and the quality of growing waters depend on the levels of E. coli or total fecal coliforms [5]. Historically, these standards have succeeded in reducing many types of shellfish-related bacterial outbreaks; however, it has been shown that the bacterial standards are inadequate for estimating the presence of enteric viruses and other chemicals in shellfish and growing waters [51, 189]. For instance, cases of shellfish toxins and many chemicals are monitored by state health agencies and/or those responsible for fish and wildlife on a regular basis (e.g., weekly or biweekly), and harvests and growing areas are placed under temporary closure based on these cell density thresholds until toxin testing in shellfish can be performed. However, in some cases, direct measurement of the hazard is not effective because analytical procedures are too slow or resource intensive, and measurement of indicators is more appropriate. In an effort to provide early warning, predictive models incorporating climate and ocean conditions such as rainfall, water temperature, and salinity are under development for control of hazards, including harmful algal blooms and naturally occurring pathogens such as Vibrio spp. [102].

The Food and Agriculture Organization of the United Nations (FAO) is recommending a food-chain approach that encompasses the whole food chain from primary production to final consumption. In such a system, the responsibility for a supply of food that is safe, healthy, and nutritious is shared along the entire food chain by all involved in the production, processing, trade, and consumption of food. Stakeholders include farmers, fishermen, processors, transport operators (raw and processed material), and consumers, as well as governments, obliged to protect public health. In order to protect public health and facilitate international food trade, the member countries of the World Trade Organization (WTO) have signed the sanitary and phytosanitary (SPS) agreement, which emphasizes the need to apply risk analysis as a basis for taking any SPS measure. Despite improvement in several countries, aquaculture governance remains problematic in others. Lack of or limited accountability by the public and private sectors, inadequate law enforcement (where regulations exist), poor planning (causing conflicts over farming sites and leading to disease outbreaks and ecosystem deterioration), and failure to address the negative environmental and public welfare impacts of some aquaculture systems result in a tarnished image and public mistrust of the industry. This is exacerbated by the lack of aquaculture-specific governance frameworks [2]. One of the most important problems faced by countries implementing biosecurity programs is the availability of government personnel to assist or oversee a number of activities that are usually considered governmental responsibilities. In many countries, a solution has been found in terrestrial and aquatic veterinary services through National Veterinary Accreditation Programs and public-private partnerships, in which the government delegates specific responsibilities to well-trained private individuals [6, 190]. For biosecurity plans to meet international standards and national or local regulations, it is wise to include procedures described in the World Organization for Animal Health (WOAH), aquatic code and manual [6, 191], and specifics in existing national or local regulations. The significance of standards set by the OIE and other international organizations, with which the OIE collaborates, is crucial for providing guidance on issues that are important to aquaculture biosecurity. It was recognized that the approach could be applied to any infectious disease, any farmed or managed aquatic species, and be implemented on any individual farm or larger contiguous areas (zones, provinces, states, countries). Furthermore, as most countries agree to adopt OIE standards in the codes and manuals, such approach would also meet most, if not all, governmental regulations [190].

At the fourth OIE Global Conference on Aquatic Animal Health (2019), a Progressive Management Pathway for Aquaculture Biosecurity (PMP-AB) was introduced by the FAO. The PMP-AB endorsed and welcomed by the tenth session of the COFI Sub-Committee on Aquaculture [192] is a ground-breaking initiative that FAO and its partners started in 2018. It is evidence-based and supported by transparent and ongoing review, adaptable to respond to the diversity of aquaculture systems, species, production scope, and objectives, and to environmental and anthropogenic changes that impact aquaculture production [193]. The approach can be applied to manage risks in any aquaculture sector, no matter the species, environment, production system, management strategy, or operation size [2]. It was developed as an extension of the progressive control pathway (PCP) approach, which has been internationally adopted to assist countries in developing systematic frameworks for planning and monitoring risk reduction strategies for the diminution, elimination, and eradication of major livestock and zoonotic diseases. The PMP/AB can guide countries toward achieving sustainable biosecurity in aquaculture and health management systems through risk-based, progressive, and collaborative processes at the regional, national, local sector, and enterprise levels. The PMP-AB consists of four stages that might lead to a sustainable and resilient national aquaculture system: (1) risk assessments, (2) biosecurity system initiated (managed in specific sectors/compartments), (3) biosecurity systems and preparedness enhanced (management system), and (4) sustainable biosecurity and health management systems established (national aquaculture system). Moving from one stage to another should meet a set of minimum requirements and a detailed implementation plan and serve as a template that may provide a degree of consistency between participating countries or regions.

5. Alternative aquaculture systems for safety farmed oysters

In the coming years, aquaculture needs to expand sustainably to fill the gap in global demand for aquatic foods, especially in food-deficit regions, and to support poverty alleviation and food security while generating new or existing sources of income and employment. This requires updating aquaculture governance by promoting improved planning, legal and institutional frameworks, and policies. FAO and partners must focus on the urgent need to develop and transfer innovative technologies and best practices to create efficient, resilient, and sustainable farms.

In the new technological age, remote inspection to ensure product safety has proven to be reliable in delivering the necessary sanitary certificates to operators. Electronic certification systems can improve traceability throughout the supply chain, reduce delays and costs, reduce food waste by speeding up the process, combat fraudulent practices by introducing electronic authentication methods, and increase trust between trading partners. To improve current practices, Codex Alimentarius is revising its guidelines to expand official certification to include an electronic certificate. In addition, electronic food surveillance reporting portals provide an effective tool for authorities to share real-time information on actions taken when serious risks are identified and help countries respond more quickly and in a more coordinated manner to health threats. In this context, FAO is exploring possible solutions through the Digital Solutions in Support of Improved Official Food Control Services project, which focuses on strengthening national capacity to develop and implement reporting portals, in addition to conducting remote inspections, supporting distance learning on food safety management, and expanding data pools to support the ongoing development of risk categorization frameworks and other risk-based decision-making tools [2].

Another approach is the “Blue Transformation,” which is committed by FAO and is a visionary strategy that aims to enhance the role of aquatic food systems in feeding the world’s growing population by providing the legal, policy, and technical frameworks required to sustain growth and innovation [2, 194]. It focuses on sustainable aquaculture expansion and intensification, effective management of all fisheries, and upgraded value chains. Blue Transformation proposes a series of actions designed to support resilience in aquatic food systems and ensure fisheries and aquaculture grow sustainably while preserving aquatic ecosystem health, preventing pollution, and protecting biodiversity and social equality. Climate- and environmentally-friendly policies and practices and technological innovations are critical building blocks for the Blue Transformation. Proactive public and private partnerships are needed to improve production, reduce food loss and waste, and increase equitable access to lucrative markets. In addition, aquatic foods need to be included in national food security and nutrition strategies, and initiatives need to be taken to raise consumer awareness of their benefits to improve availability and access.

In addition, WHO promotes safe food-handling practices worldwide and ensures consistency in their application throughout the food chain from farm to table. One of WHO’s priorities is to reach people who usually do not have access to food safety training despite the important role these people often play in producing safe food for the community, in which they live [98]. Efforts have been initiated to educate consumers, restaurant proprietors, and physicians about the hazards of eating oysters. In 2001, WHO launched the Five Keys to Safer Food campaign to highlight practices needed to ensure safe food preparation in small grocery businesses and the home. The concept reinforces the One Health approach, which seeks to promote an understanding of the relationships between the health of humans, animals, and the environment and the mechanisms by which noncompliance with good hygiene practices in one sector can affect other sectors. Adopting effective food safety practices in aquaculture and handling will impact overall hygiene and environmental behaviors, improving community health, protecting the environment, and reinforcing sustainable development. The Five Keys to Safer Food poster has been translated into over 90 languages and has been the starting point for numerous national and local food safety training programs. WHO has expanded the Five Keys to Safer Food program to include more groups and sectors involved in the farm-to-table chain. The core messages of the Five Keys to Safer Food are: (1) keep clean, (2) separate raw and cooked, (3) cook thoroughly, (4) keep food at safe temperatures, and (5) use safe water and raw materials.

Without a doubt, one of the strongest recommendations is one of the key messages of the Global Conference on Aquaculture 2020, which argues that “prevention is better than cure.” Focusing on prevention is a sign of a maturing industry. Use of clean seed with good husbandry practices and biosecurity strategies in a less stressful and healthier aquatic environment are basic actions. Biosecurity measures implemented proactively and preventatively are much less expensive than reactionary responses to outbreaks, and they should be integrated with aquaculture development by all producing countries. Effective biosecurity, best husbandry practices, good genetics, and quality nutrition are important for producing healthy, nutritious, and resilient farmed organisms [195, 196].

6. Final remarks

Aquaculture has long been an important food source and livelihood for millions worldwide. However, if these products are not handled, stored, and processed correctly, their safety may be affected due to contamination by different agents. Sewage and animal waste contamination of oysters harvesting areas probably represent the most significant contributing factor in human cases of oyster-associated diseases. Also, oysters can cause foodborne diseases with seafood processing through inadequate operatives or systems of hygiene practices. Of all available seafood commodities, live and raw oysters are among the riskiest products consumed by humans, although cooked oysters have also been implicated. Among the seafood, hazards include bacterial and viral pathogens, parasites, marine toxins, heavy metals, and other chemical contaminants from anthropogenic sources, such as pesticides and pharmaceuticals. Outbreaks of oyster and other bivalves-associated infections have been reported for over a century. Most infectious syndromes produce self-limiting gastrointestinal symptoms, but a few can be fatal. In the last decades, the global consumption of shellfish has increased considerably, as well as the reports of outbreaks of infection.

Some hazards that have been introduced preharvest can increase following postharvest handling, whereas others may be effectively mitigated. Additional hazards may be introduced postharvest, during production, or processing, and vary considerably among seafood commodities. Oyster commercialization needs to be careful with biosecurity and disease control, which must be coupled with effective management from aquaculture production to distribution to different sectors. Thus, the application of risk analysis to the aquaculture sector has become very important. The oyster industry has agreed that the most effective way to control risks is through the implementation of programs, manuals, and procedures for good hygiene and sanitation practices, as well as sanitation standard operating procedures. Those are part of the prerequisite programs established as the basis for implementing stricter methodologies whose main objective is to guarantee food safety and quality of novel foods considering addressing the specific implications for consumer protection, public health, and trade. Thus, the application of risk analysis and the implementation of hazard analysis critical control point plans have become very important worldwide and necessary to address proper harvest, storage, and processing procedures. With the adoption of the food-chain approach for food safety, the responsibility for the supply of safe, healthy, and nutritious seafood is shared along the entire food chain from producer to consumer. For this reason, it is imperative to implement and apply safety systems, such as good practices, to prevent or reduce the risks of contamination in food, thus contributing to the maintenance of its quality and safety, providing consumers with sustainable and secure seafood.