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Abstract
Review The Prevalence of Viruses Related to the Production of Mussels and Oysters in Saldanha Bay: A Systematic Review 1 , 1 2 1 Likentso Sylvia Shuping * , Izanne Susan Human , Jan Frederik Rykers Lues and Arnelia Natalie Paulse Department of Environmental and Occupational Studies, Faculty of Applied Science, Cape Peninsula University of Technology, Cape Town 8000, South Africa Centre for Applied Food Sustainability and Biotechnology, Central University of Technology, Bloemfontein 9301, South Africa * Correspondence: shupingl@cput.ac.za; Tel.: +27-711980508 Abstract: The disposal of treated and untreated sewage near shellfish harvesting areas is a global concern. Discharged sewage may be contaminated with enteric viruses present in human faeces. Bivalve molluscs, in turn, act as vectors for enteric viruses through bioaccumulation and retention of these viruses during the filter-feeding process, resulting in outbreaks of infections due to the consumption of contaminated shellfish. This review was conducted using peer-reviewed articles published from 2012 until September 2022, obtained from online databases such as Google Scholar, Scopus, and Science Direct, highlighting the challenges that the shellfish industry is faced with concerning pollutants ending up in the shellfish production areas. Developed countries have made some advancements by upgrading sewage infrastructures, which reduced viral loads in sewage. However, it is difficult to measure the significance of these improvements, as there are no regulations in place which stipulate the permissible limits for viruses. In most developing countries, including South Africa, there is a lack of effective management plans for virus monitoring in shellfish harvesting areas. The findings of this study indicated a need for extensive research on the origin of viruses, their interactions with other organisms within the marine ecosystem, the quantification of viruses within the Saldanha Bay harbour, and the development of virus management plans which currently are non-existent. Citation: Shuping, L.S.; Human, I.S.; Lues, J.F.R.; Paulse, A.N. The Keywords: shellfish; production areas; norovirus; hepatitis A; enteric viruses Prevalence of Viruses Related to the Production of Mussels and Oysters in Saldanha Bay: A Systematic Review. Aquac. J. 2023, 3, 90–106. https:// 1. Introduction doi.org/10.3390/aquacj3020009 The shellfish farming industry has seen exponential growth worldwide, providing Academic Editors: Haohao Wu and an alternative source of protein needed for the growing world population [1,2]. Shellfish Aires Oliva-Teles farming is conducted in rivers, estuaries, and open seas. In open seas, the ideal location is a sheltered embayment, often surrounded by residential and industrial areas. However, the Received: 14 December 2022 challenge is the protection of shellfish farms or production areas from contamination [3]. Revised: 16 March 2023 Production areas are subjected to the discharge of treated and untreated sewage, which may Accepted: 6 April 2023 be loaded with bacteria and viruses, as well as wastewater disposal from industries nearby, Published: 13 April 2023 which may be loaded with chemicals and heavy metals [4–6]. Enteric viruses are widely spread in soil, water, and food. Viruses are also excreted in large quantities in the faeces of infected individuals (up to 10 viral particles per gram of stool) [7] and are persistent in Copyright: © 2023 by the authors. the environments where they are found [8]. Some of the enteric viruses of concern include Licensee MDPI, Basel, Switzerland. norovirus Genogroup I and Genogroup II (NoV GI and GII); hepatitis A (HAV); rotavirus This article is an open access article (RV), astrovirus (AsV); sapovirus (SaV), adenovirus (AdV), aichivirus (AiV), and Hepatitis distributed under the terms and E (HEV). The SaV, AiV, and HEV are regarded as emerging viruses [9,10]. Norovirus (NoV) conditions of the Creative Commons is regarded as the most common cause of acute and nonbacterial gastroenteritis in humans Attribution (CC BY) license (https:// and is implicated in most shellfish-borne viral outbreaks [11]. Furthermore, NoV is reported creativecommons.org/licenses/by/ as the major causative agent in foodborne outbreaks in European countries after Salmonella 4.0/). Aquac. J. 2023, 3, 90–106. https://doi.org/10.3390/aquacj3020009 https://www.mdpi.com/journal/aquacj Aquac. J. 2023, 3 91 bacteria. It was also associated with 457 outbreaks in 2019 in Europe [12], with oysters being the most implicated bivalve molluscs in foodborne outbreaks [13–16]. Hepatitis A (HAV) has also been reported as a cause of foodborne diseases [17], and a common cause of acute hepatitis infections worldwide with mild illnesses [18]. It is transmitted through the faecal-oral route from person to person or through the consumption of contaminated food or water. The biggest outbreak of HAV was in Shanghai in China in 1988, which was attributed to the consumption of raw clams [18]. Improved hygiene conditions and the introduction of the Hepatitis A vaccine caused a decline in cases until recently, in 2020 when an outbreak occurred in Yantai, which also implicated the consumption of contaminated shellfish. Other foods such as frozen berries have been implicated in an outbreak of HAV in Italy in 2013–2014 [19]. The Hepatitis E virus is a major cause of acute hepatitis in humans. Approximately 17 outbreaks have been reported in Africa annually since 1979 resulting in 650 deaths [20]. Pregnant women are at an increased risk of developing complications with HEV infection that could lead to fulminant hepatic failure [21]. Bivalve molluscs, including oysters and mussels, feed on suspended materials in their growing waters. They filter large quantities of water, subsequently accumulating and retaining contaminants available that are bound to the suspended materials [10]. Shellfish, apart from being a good source of protein and rich in micronutrients, play an important role in the marine environment as they purify water, thereby reducing eutrophication [22]. The nature of filter feeding is a public health concern as contaminants such as viruses can pose a health threat to shellfish consumers. Moreover, disease outbreaks where shellfish contaminated with enteric viruses are consumed are exacerbated by the norm of eating shellfish raw or partially cooked [23–25]. Sources of contaminants including sewage outfall, illegal wastewater discharge, stormwater discharge, heavy rainfall, agricultural runoffs, overboard disposal of faeces from boats, river flows, informal settlement dwellers, and natural disasters such as hurri- canes and flooding increase the risk of contamination of shellfish growing areas [26–29]. Even though the available literature is mainly from other parts of the world, 17 studies were conducted on enteric viruses in shellfish over the past two decades in Africa [30]. In South Africa, studies were conducted on the contamination of rivers by enteric viruses [31–34]. Only a few studies are available on the contamination of shellfish by viruses and none so far explored virus contamination in Saldanha Bay [35]. Contaminants affecting Saldanha Bay shellfish farms are primarily from port operations (export of metal ores), ships traffic, ballast water discharge, oil spills, municipal sewage discharge, industrial effluent (brine, cooling water discharges, fish factory effluent), and stormwater discharge which may contain enteric viruses [36]. Impact of Enteric Virus-Contaminated Shellfish on Public Health Norovirus has been implicated in 14–23% of global infections due to the consumption of contaminated shellfish. It is also responsible for 125 million foodborne illnesses and 35,000 deaths in a year [23]. Norovirus has six genogroups (GI–GVI), with genogroups I, II, and IV associated with human gastroenteritis infections. In the United Kingdom (UK), approximately 74,000 NoV cases due to the consumption of contaminated foods and 11,800 due to the consumption of contaminated oysters are reported annually [37]. Clinical symptoms include headache, fever, diarrhoea, abdominal cramps, and nausea. Clinical symptoms related to HAV infections include jaundice, diarrhoea, abdominal pain, fever, malaise, and loss of appetite, with 1.4 million cases reported globally per annum [38]. It can also cause acute liver failure which may be fatal [39]. Studies conducted on HAV-contaminated foodstuffs have only contributed to 2–7% of all the food-related outbreaks worldwide, and are also reported as less common in bivalve molluscs compared to NoV [39,40]. Hepatitis E is receiving attention in food contamination as it affects 20 million people per annum with 56 600 deaths [41]. It is regarded as an emerging zoonotic foodborne threat [42]. Shellfish consumption is implicated in transmitting HEV in Asian countries such as China, Japan, Korea, and Thailand. In Vietnam, it has been detected in shellfish Aquac. J. 2023, 3 92 samples [40]. A few cases have also been reported in European countries, as well as the Netherlands, Spain, and the UK [9,40,41]. In Italy, HEV has not been detected in shellfish- approved harvesting areas [40]. In the African continent, HEV is a waterborne disease that is transmitted through faecal contamination of water and poor sanitation and hygiene. The lack of specific HEV surveillance in most African countries makes it difficult to monitor trends in disease incidence and identify outbreaks [21,43,44]. Aichivirus was reported in 1989 in Japan as the cause of oyster-associated nonbacterial gastroenteritis [45]. Sapovirus was first detected in an outbreak which occurred at an orphanage in Japan in 1977 and was detected in 3 out of 11 outbreaks in Japan which occurred between 2002 and 2006, due to the consumption of contaminated oysters [46,47]. Outbreaks are also common among children [47]. Rotavirus causes acute diarrhoea in children under 5 years of age, with clinical symptoms including diarrhoea, anorexia, dehydration, and occasional vomiting [17]. Clinical symptoms relating to Astrovirus infections include occasional vomiting, fever, abdominal pain, and anorexia. It has been detected in mussels and oysters, even though fewer outbreaks have been reported [48]. Rotavirus is one of the main causes of childhood diarrhoea worldwide. It has not been linked to gastroenteritis outbreaks related to seafood; neither has adenovirus [49]. Table 1 shows some of the documented foodborne disease outbreaks due to viral infections. Table 1. Enteric viruses associated with shellfish disease outbreaks. Enteric Virus Country and Year Bivalve Mollusc References France, 2012 Oyster [50] Canada, 2016 Oyster [16] Norovirus US, 2009–2014 Oyster [15] (GI and GII) South Korea, 2013 Oyster [51] France, 2019 Oyster [52] Hawaii, 2016 Scallops [53] China, 1988 Clams [18] Hepatitis A China, 2020 Oyster [18] Italy, 1997–2004 Raw shellfish [54] Australia Oysters [17] Aichivirus Japan, 1989 Oyster [13] Sapovirus Japan, 1977 Oyster [46] The rapid increase in cases but not frequently Astrovirus, adenovirus, Rotavirus implicated in outbreaks occurrence [9,48] Apart from the contaminants mentioned above, there are currently contaminants described as emerging contaminants (pharmaceutical products, personal care products, antibiotics, surfactants, artificial sweeteners, flame retardants, cleaning solvents, sun pro- tection products, etc.), including microplastics. Their presence in the marine ecosystem is a concern for the health of marine organisms. They are aggressive in nature, have toxic effects and the ability to bioaccumulate, and are not effectively removed from sewage by traditional wastewater treatment methods [55]. Microplastics may act as vectors for the spread of antimicrobial-resistant genes, harmful microorganisms, and as a microcosm for gene exchange between bacteria [56–58]. The microbiological monitoring programme in Saldanha Bay is well-established in the monitoring of bacterial contamination, but lacking in virus contamination monitoring. This review aims to gather epidemiological data available on virus contamination at shellfish harvesting areas. The existing data could assist with relevant information for policy-makers to consider when developing policies and strategies for managing virus contamination in Saldanha Bay. Aquac. J. 2023, 3, FOR PEER REVIEW 4 Aquac. J. 2023, 3 93 2. Materials and Methods 2. Materials and Methods For this desktop review, all literature on virus contamination in shellfish harvesting For this desktop review, all literature on virus contamination in shellfish harvesting areas worldwide was included. The literature search was conducted using online elec- areas worldwide was included. The literature search was conducted using online electronic tronic databases such as Science Direct, Scopus, and Google Scholar with a timeframe of databases such as Science Direct, Scopus, and Google Scholar with a timeframe of 2012 and 2012 and 2022 to ensure that the latest information was included. However, there were no 2022 to ensure that the latest information was included. However, there were no timeframe timeframe restrictions on the introduction and discussion sections. The Boolean logical restrictions on the introduction and discussion sections. The Boolean logical connectors connectors (‘AND’ and ‘OR’) and truncation were applied in the search strategy. The (‘AND’ and ‘OR’) and truncation were applied in the search strategy. The search terms search terms were mussels and oysters AND hepatitis A and “norovirus GI and GII” AND were mussels and oysters AND hepatitis A and “norovirus GI and GII” AND production production areas OR shellfish farms OR growing waters AND sources. The following in- areas OR shellfish farms OR growing waters AND sources. The following inclusion and clusion and exclusion criteria were used: the original articles writt en in English from peer- exclusion criteria were used: the original articles written in English from peer-reviewed reviewed journals and the prescribed timeframes were included. Unpublished papers, journals and the prescribed timeframes were included. Unpublished papers, theses, non- theses, non-peer-reviewed articles, articles on mussels and oysters from wholesale and peer-reviewed articles, articles on mussels and oysters from wholesale and retail markets, retail markets, food processing, post-harvest treatments, book chapters, and abstracts food processing, post-harvest treatments, book chapters, and abstracts were excluded. The were excluded. The exclusion and inclusion criteria were strictly followed to reduce the exclusion and inclusion criteria were strictly followed to reduce the risk of biases. Two risk of biases. Two reviewers worked together to screen records and retrieve reports. A reviewers worked together to screen records and retrieve reports. A report was retrieved report was retrieved from the Scopus database. Reports were not available for retrieval from the Scopus database. Reports were not available for retrieval from Google Scholar from Google Scholar and Science Direct. Records screened from Google Scholar and Sci- and Science Direct. Records screened from Google Scholar and Science Direct that met the ence Direct that met the inclusion criteria were saved in the Google Scholar library of one inclusion criteria were saved in the Google Scholar library of one of the reviewers. The of the reviewers. The screening, evaluation, and identification of records for eligibility screening, evaluation, and identification of records for eligibility were conducted following were conducted following the Preferred Reporting Items for Systematic Review and Meta- the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) flow diagram Analysis (P (Figur RISMA e 1))[ 59 flow d ]. iagram (Figure 1) [59]. Figure 1. PRISMA methodology of literature search (available from: htt p://www.prisma-state- Figure 1. PRISMA methodology of literature search (available from: http://www.prisma-statement. ment.org, accessed on 6 September 2022). org, accessed on 6 September 2022). Aquac. J. 2023, 3 94 3. Results A total of 181 records were identified through a database search. After screening the records and looking at titles, abstracts, and duplicates, 147 records were excluded. Full texts of the remaining 29 were scrutinised for eligibility and 10 records were excluded. Nineteen records were retained for qualitative synthesis (Figure 1). Table 2 summarises the findings and recommendations of the studies that were in- cluded in this review. Most of the studies implicated sewage discharge in shellfish growing areas as the source of enteric virus contamination. Therefore, they recommended the development of effective management plans for shellfish harvesting areas, and the devel- opment of virus compliance limits as well as virus indicator species, since the use of E. coli has proved to be ineffective in detecting viral contaminants. Table 2 also represents the literature available on enteric viruses’ contamination in shellfish harvesting areas and the studies conducted according to the search keywords used per country. The data search was from 2012 until September 2022, the studies conducted per country are as follows: Britain (1); Italy (6); Australia (1); England and Wales (1); Montenegro Coast (1); Brazil (3); France (1); Argentina (1); Spain (1); Poland (1); Korea (1); and Morocco (1). These studies included Hepatitis A, norovirus, and other emerging viruses, with a focus on contamination in harvesting areas. Most of the studies conducted were on oyster contamination with the most implicated virus being norovirus. Table 2. Summary of studies included in the review that met all the criteria specified. Study Area Aim of the Study Findings Recommendations References Geographical and temporal variations (1) High concentrations (1) To determine the must be considered in of NoV on sampling impact of geographical harvest area sites close to the and temporal changes monitoring sewage discharge point. Poole Harbour, Britain on E. coli and norovirus programmes and most [11] (2) Higher in mussels. importantly concentrations of E. coli (2) Influence of incorporated into food in mussels than in environmental factors. safety regulations and seawater. harvest area management plans. (1) Development of strategies and methodologies to assess public health risks. Detection of enteric Assessment of enteric (2) Systemic controls viruses indicates they viruses including HAV for viral pathogens to Syracuse, Italy are widely distributed [8] and NoV in bivalve protect consumers. in aquatic molluscs. (3) An integrated environments. surveillance system reporting food safety, environmental exposure, and clinical cases. Oysters demonstrated a Efficient monitoring of possible link between Determine existence of harvest areas to chemical pollutants a relationship between determine a correlation Gulf of Pozzuoli, Italy and the [10] viral and chemical between environmental bioaccumulation of contamination. pollutants and multiple enteric foodborne viruses. viruses. Aquac. J. 2023, 3 95 Table 2. Cont. Study Area Aim of the Study Findings Recommendations References (1) Stringent shellfish monitoring (1) Detection of E. coli, programmes. HAV and NoV in (2) Inclusion of Norovirus was shellfish samples. environmental Sardinian shellfish prevalent in all areas (2) Assessment of parameters. [60] farms, Italy during the winter possible relationships (3) Improved season. between pathogens and monitoring plans could seasonality. lead to better management of shellfish harvest areas. Underreporting of Evaluate NoV and viruses’ occurrence in The development of HAV occurrence in wild shellfish could viral indicators such as wild Baltic mussels and Baltic Sea, Poland limit insight into the E. coli is not effective in [61] possible inclusion as role they play in the prediction of viral indicator species for environmental viral pollution. viruses. transmission. An increase in viral The human population Assess the occurrence contaminations calls for Australia, New South around the shellfish of NoV and E. coli in control measures Wales, Tasmania and growing areas is lower [7] Pacific oysters and specific to virus South Australia in Australia compared Sydney rock oysters. pollution in to other countries. shellfish-growing areas. Viruses-specific control measures are required for monitoring Heavy rainfall was Commercial harvesting Determine the possible harvesting areas. implicated in high areas- coast of England predictor variables for Improvement of [62] concentrations of E. coli and Wales NoV in oysters. sewage infrastructure levels. and improvement of risk management measures. Integration of To establish a The presence of microbiological and relationship between chemical contaminants chemical monitoring Campania region, Italy environmental [63] influenced viruses’ programmes as an parameters and viral bioavailability. effective warning contamination. system. Evaluate the effects of Consumer awareness Confirmed circulation the different enteric campaigns on the Gulf of Naples, Italy of multiple enteric [63] viruses within bivalve importance of cooking viruses in bivalves. molluscs. seafood thoroughly. Seasonality and the (1) Improvement of To determine the human population shellfish monitoring distribution rate of Montenegro Coast contribute to the programmes. [64] NoV in mussels along prevalence and spread (2) Development of the coast. of viruses. virus-specific criteria. Aquac. J. 2023, 3 96 Table 2. Cont. Study Area Aim of the Study Findings Recommendations References (1) High concentrations of HAV, NoV and AdV were detected during winter months in water, mussels, and oyster Improvement in Mangrove Estuary, Quantify enteric samples. shellfish monitoring [49] Brazil pathogenic viruses. (2) Estuary should be programmes. classified as a prohibited zone for bivalve harvesting for human consumption. (1) Prevention of NoV contamination Seasonality and high contamination. Atlantic Coast Lagoon, and gastroenteritis prevalence of NoV in (2) Development and [65] France outbreaks. oysters. implementation of an outbreak alert system. Development of a monitoring system for To develop a routine Production in Sicily, Prevalence of enteric viruses, using data monitoring plan for [66] Italy virus. from epidemiological enteric viruses. studies and existing molecular methods. Detected NoV in RvA Understanding viruses’ Southern Coast of To determine the in samples and circulation to improve Buenos Aires Province, presence of NoV and [67] resistance to heat existing surveillance Argentina RvA in oysters. treatment. plans. (1) Harvest areas affected by close Compile a database on proximity to pollutants A better understanding the prevalence of discharge points and of emerging enteric Galicia, Spain [42] enteric viruses in dilution factors. viruses’ behaviour and shellfish. (2) Role of bivalves as a pathogenicity. vector of zoonotic diseases. Investigate the (1) No commercial contamination status of NoV GII strains are the harvesting in polluted the oyster growing area most prevalent in areas. Jinhae Bay, Korea [68] by NoV and the oysters and elimination (2) Prevent faecal circulation of can be difficult. contamination in NoV genotypes. production areas. (1) Contamination by various pathogens due Florianópolis, on the To perform a thorough to sewage discharge. Control measures are coast of Santa Catarina, diagnosis of the (2) Complexities of necessary to ensure the [69] Brazil shellfish growing areas. microbiological and safety of produce. chemical compound contaminants. Mapping out the pollution sources, using Analysed the presence Mussels and oysters the findings to develop Lagunar complex of Astrovirus and NoV tested positive for the risk assessment and [48] Cananẻia, Brazil in mussels and oysters. studied viruses. control measures of pathogen contamination. Aquac. J. 2023, 3 97 Table 2. Cont. Study Area Aim of the Study Findings Recommendations References Importance of implementing a Evaluate NoV national survey plan Oualidia Lagoon, frequency in bivalve Risk of contamination and sanitary control for [70] Morocco shellfish harvested at in oysters. the viral risk, including Oualidia lagoon. NoV in bivalve molluscs. 4. Discussion Contamination of bivalve molluscs with viruses is a global concern. Vulnerable people such as the elderly and immunocompromised individuals die when foodborne outbreaks occur [23]. According to Table 2, only one study was conducted on the African continent. Urgent interventions are needed for the continent to develop food safety in the shellfish industry to the same level as other developed and developing countries. Detection of HAV and NoV indicates that these agents are widely distributed in aquatic environments [71,72]. This correlates with global trends where sewage is discharged along the coastal areas, including African countries and South Africa in particular. The findings and recommendations from the nineteen studies listed in Table 2 could be a starting point for the development of management plans for virus detection and monitoring in Saldanha Bay. The summary of findings and recommendations according to Table 2 is as follows: High concentrations of NoV at harvesting areas or sampling sites close to the sewage dis- charge point were mentioned by most of the studies. Disposal of sewage whether treated or untreated is a major challenge facing the shellfish industry globally [23,26,37,73–76]. Sewage discharge points near shellfish harvesting areas give rise to the challenge of eliminating viruses by bivalve molluscs. Pouillot et al. [76] demonstrated in their study how oysters bioaccumulated viral particles in high concentrations within a short period. They also added that through the bioaccumulation process, virus concentrations in oyster tissues exceeded the virus concentrations in the water. Similarly, Sharp et al. [75] observed high concentrations of NoV in mussels within 3 h of exposure to water contaminated with treated and untreated sewage. Souza et al. [77] added that viral particles may be 100 times more concentrated in bivalve molluscs’ organs than in contaminated seawater. To prevent contamination of commercially harvested bivalves, the United States Food and Drug Ad- ministration (USFDA) determined a prohibition zone, where bivalves may not be harvested for commercial purposes, and decided on the dilution criteria of 1000 parts of receiving waters to every part of effluent (1000:1) [78]. These were determined through comparisons of studies such as USFDA hydrographic dye dispersion and numerical hydrodynamic models to track the discharge of wastewater. The 1000:1 dilution criterion is equated to waters within a distance of 3.77 km from the sewage outfall [79]. Schaeffer et al. [80] also agree with having a buffer zone whereby shellfish harvesting is prohibited if contamination cannot be prevented. Chemical contaminants from industrial activities and runoffs from land also pose a challenge and a public health risk. The risk for consumers differs depending on the chemi- cal compounds formed by different chemicals. For example, Arsenic (As) in its inorganic form may alter tumour-suppressing genes and has been classified by the International Agency for Research on Cancer (IARC) as cancer-causing in humans [81]. Fiorito et al. [59] in their studies observed a correlation between chemical pollutants and viral contaminants in mussels. The mussels that tested positive for viral presence exhibited higher levels of chemical pollutants than the mussels that tested negative for viral contaminants. The higher the exposure to chemical agents, the weaker the immune system and thus the higher the uptake of microbial agents [82]. The effects of having both biological and chemical contam- inants need to be explored further to ascertain a possible link between chemical pollutants and the bioaccumulation of multiple enteric viruses in bivalve molluscs [59]. Adding to Aquac. J. 2023, 3 98 the burden of chemical contaminants are microplastics, which are considered emerging pollutants. Owing to their small size, they can be mistaken for food by bivalves. Some studies demonstrated that mussels and oysters ingest microplastic particles from the sur- rounding seawater [83]. Although the potential for human viruses to attach to microplastics and to persist in the plastisphere is unclear [83], Moresco et al. [58] indicated that biofilm on surfaces of plastics could provide a platform for viral attachment. Yamada et al. [84] agreed with the suggestion that microplastics could be potential adsorbents for viruses. However, they added that more research is needed on the influence viruses have when attached to biotic and abiotic particles in marine ecology, as well as the extent to which these attached viruses are infective to their hosts. On the other hand, it is well established that microplastics can provide a habitat for the colonization and enrichment of Vibrio species and vectors of pathogenic bacteria including Pseudomonas and Acinetobacter [85]. The danger lies in the possibility of microplastics being a vehicle for the spread of infection in aquaculture which could have a detrimental economic impact [56]. Bivalve production sites are mostly situated along the coastal areas [27,86,87], where possible exposure to sewage contaminated with human enteric viruses is high. Bivalves act as zoonotic disease vectors through the bioaccumulation process when filtering the water in their growing areas. The concentration and retention of enteric viruses for long periods pose a public health threat as bivalves are commonly eaten raw or partially cooked, particularly oysters [37]. Coastal areas are becoming more attractive for residential developments and tourism (which is important for the coastal economy) as some are secluded and bring about peace and quality of life away from densely populated suburban metropolitan areas [88]. Such developments bring an increase in activities such as boating, snorkelling, fishing, and many more activities which may introduce pollution into the ocean near the developments [89]. To meet the demands of the human population increase, agricultural lands are converted into residential and industrial developments, leading to altered water quantities and quality, as well as altered sediment which ultimately lands in the ocean, increasing faecal microbial loads, and nutrients [4]. El Mahrad et al. [90] reported and described changes that are brought about by human influx in a coastal city in Morocco, including alteration of sedimentary forms especially the dunes on the east side of the lagoon. Furthermore, changes in ocean chemistry may cause ocean acidification, changes in precipitation, a rise in sea levels, and changes in seawater pH [91]. Increased inputs of nutrients could trigger harmful algal blooms [92]. A summary of the recommendations is as follows: Geographical and temporal variations must be considered in monitoring programmes of harvesting areas and incorporated into regulations or harvesting area management plans. The environmental factors within the harvesting areas play a role in microbial pollutants’ prevalence [60]. Strubbia et al. [11] observed high microbiological contamination at a site that was receiving large amounts of sewage discharge and concluded that such events must be taken into consideration for monitoring harvesting areas. Microbial pollutants are not the only aspect affected by geographical and temporal variation, marine biotoxins also show similar trends. Goya et al. [93] identified temporal variability with paralytic shellfish poisoning toxins which were higher in summer months, lower in winter, and lowest in autumn. According to Wu et al. [94] regional and seasonal differences were observed, where some biotoxins bloomed during the upwelling season and some during the downwelling season. Spatial and temporal variability could also be due to coastal natural processes and local changes in environmental conditions [95]. There seems to be a consensus about the lack of effective management plans or strate- gies in shellfish harvesting areas [10,11,42,56,64]. Some researchers also highlighted the need to have an integrated surveillance system that will enable simultaneous reporting on environmental exposure and clinical cases to facilitate tracking and correlation of occur- rences of clinical cases with environmental factors in harvesting areas [8]. La Rosa et al. [43] agreed with the concept of an integrated surveillance system and added that it could be useful to monitor changes in viral patterns and could offer a warning of contamination in Aquac. J. 2023, 3 99 advance. Some researchers also recommended the inclusion of environmental parameters in shellfish management plans for the correlation between meteorological events and the prevalence of viruses. Furthermore, the development of viral indicators [96] is required, as E. coli is not effective in the prediction of viral pollution as it has lower environmental resistance than viral pathogens [11]. Sharp et al. [75] demonstrated in their study how oysters accumulated E. coli and norovirus in their bodies and how both microorganisms responded to depuration, with E. coli being successfully purged from the shellfish tissues within 72 h but failed to remove norovirus from the shellfish tissues. Several studies proposed the use of bacteriophages as indicator species for viral contamination. Others proposed the use of norovirus as an indicator species [7,26,64,75,97]. The traditional way of eating bivalve molluscs, i.e., raw or undercooked, appears to be a health risk and consumer awareness is necessary. Consumers are perceived to be aware of chemical hazards in food as they cause long-term adverse effects including cancer and are less concerned about microbial hazards [98]. Ricardo et al. [99] added that it is important to precisely know the bivalve origin and the sources of pollutants considering their sedentary lifestyle and feeding behaviour. They bioaccumulate pollutants, which is exacerbated by how they are eaten (raw or undercooked), leading to the risk of transmission of infections to humans. More studies on foodborne outbreaks associated with shellfish consumption will increase consumer awareness [100]. Crovato et al. [101] evaluated studies that conducted research on shellfish consumption and reported that consumers were confused about the risks and benefits of bivalve molluscs. They concluded that accurate information is necessary for helping consumers to make informed choices. In addition, Fiorito et al. [63] highlighted the importance of awareness campaigns to inform consumers of the thorough cooking of seafood. This remains a challenge as people prefer eating oysters raw and mussels lightly cooked [102]. Evaluation of sources of pollutants is the first step that may lead to effective man- agement of shellfish harvesting areas. Knowing what pollutants are present, where they come from, and their composition will enable policymakers to develop management plans and monitoring programmes accordingly [48]. For example, Mok et al. [102] evaluated the bacteriological seawater quality and oyster quality from a coastal area in Japan, where they conducted a sanitary survey to analyse all the possible sources of pollutants. The study concluded that faecal coliform levels were high after heavy rainfall events compared to other sampling occasions. Therefore, it was reported that oysters are safe to be consumed raw during dry seasons based on their bacterial water quality. Chinnadurai et al. [103] similarly evaluated seasonal occurrences of faecal coliforms and found elevated levels dur- ing monsoon periods, and therefore suggested that authorities develop sanitary control in line with international standards, as no microbiological standards existed. The prevalence of viruses is influenced by seasonality. Several studies reported high concentrations of NoV during the winter season when heavy rainfall occurred [65,74,76,104–107]. Lower concentrations were measured in summer months with low rainfall, which is suggested to be due to the inactivation of viruses by sunlight and viral clearance because of the high metabolic rate in summer [12]. A sanitary survey process identifies and evaluates all environmental factors and actual and potential sources of pollution that could harm the water quality of shellfish growing waters [103]. The National Shellfish Sanitation Program [78] outlines what a sanitary survey must entail which includes conducting a shoreline survey, and a survey of the microbiological quality of the water. In addition, an evaluation of the effect of any meteorological, hydrody- namics, and geographic characteristics on the growing areas will assist in determining the appropriate growing areas’ classification. Once a sanitary survey exists, it must be updated or reevaluated every three years. An annual review based on meteorological and hydrody- namics should also be performed to ensure that conditions are unchanged. Regulations have been developed internationally, regionally, and locally to specify acceptable levels of bacterial pathogens in shellfish tissues or in water where shellfish are grown. This has led to the classification of production areas for shellfish harvest fit for human consumption [108]. Aquac. J. 2023, 3 100 Standards are available for the detection of HAV and NoV in some food groups, which would eventually lead to the establishment of regulations where set compliance limits for enteric viruses in shellfish are specified [109]. Emerging viruses must also be prioritised due to the rapidly increasing number of cases associated with them [71]. As mentioned, the presence of viruses in food is a global concern, with viruses such as norovirus and Hepatitis A causing foodborne outbreaks [9]. Further studies are needed on the occurrence, behaviour, and genotype distribution of emerging enteric viruses in the environment, their epidemiology, temporal and geographi- cal distribution, environmental stability, and potential health risks to humans [64,110]. Effective risk management strategies need to focus on the prevention of contamina- tion [107]. The European Food Safety Authority (EFSA) recommended that contamination should be prevented in the first instance, which might be achieved by ensuring viral treat- ment of sewage or growing oysters sufficiently distant from sewage outflows (European Food Safety Authority, 2019) [111]. Shin et al. [68] are of the same view that the most effective control measure is to prevent faecal contamination in oyster production areas or to restrict commercial harvesting from contaminated production areas. Campos et al. [64] emphasised that if this recommendation was to be successful or effective, it would require a good understanding of the environmental factors influencing the movement of NoV and other enteric viruses within the hydrological catchments and integration of microbiological and chemical monitoring programmes for effective warning systems. Written management plans are required for each shellfish growing area. Detailed reports on characteristics of effluent discharged near shellfish growing areas, dilution factors depending on the clas- sification of growing areas, determining the distance from the pollution sources to the growing areas, and the impact of each source on the growing area should be compiled [78]. Several studies have shown that world population growth and urban developments have a detrimental impact on the microbiological quality of freshwater ecosystems and marine ecosystems [4,62,97,112,113]. Webber et al. [114] in their study detected the presence of NoV, AdV, and RT in shellfish farms and found that the treatment of sewage did not provide effective removal or elimination of pollutants. Garbossa et al. [112] also reported in their study that shellfish farms are at risk of being contaminated with enteric viruses which are transported to the farms through sewage discharge and indicated that the current wastewater treatment plants are not designed to effectively remove enteric viruses. Trottet et al. [28] and Hassard et al. [23] recommended upgrades of existing wastewater treatment plants, effluent pipes, or shellfish bed relocation based on principles of dilution factors’ zoning. Campos et al. [115] tested the effectiveness of faecal coliform load reduction after the improvement of a sewage treatment plant’s infrastructure and observed a reduction in E. coli concentrations with the greatest reduction identified at a site more distant from sewage discharges. The available literature is mostly from developed countries and some developing coun- tries (Table 2). The available literature on the African continent shows that only 17 studies were conducted in the past two decades in detecting enteric viruses in Africa [30]. In Sal- danha Bay, on the West Coast of South Africa, where both mussels (Mylitus galloprovincialis) and oysters (Crassostrea gigas) are farmed, monitoring of bacteriological contamination is conducted, while monitoring of enteric viruses is lacking. The findings of this review highlight the importance of monitoring enteric viruses for the safety of public health, and therefore, may serve as a baseline for the development of a management plan for enteric viruses in Saldanha Bay, Western Cape, South Africa. 5. Conclusions This review provides information on the global prevalence of enteric viruses in studies conducted between 2012 and 2022 in shellfish production areas. The findings confirm that shellfish contamination happens in harvesting areas that are subjected to the discharge of treated and untreated sewage continuously or intermittently. Several studies are of the view that the effective control measure for viral contamination is to harvest shellfish Aquac. J. 2023, 3 101 in areas that are not faecally contaminated and encourage the development of effective viral management plans for shellfish harvest areas. Quantification of the virus community in Saldanha Bay Harbour is crucial as well as quantification of existing pollutants and emerging pollutants to develop comprehensive strategies in the management of viruses as contaminants for bivalve molluscs. This study will serve as a baseline for the shellfish industry in South Africa to consider monitoring viruses and developing management plans for viruses. Before the development of management plans for viruses, extensive research is needed in understanding viruses’ origins, the influence brought by interaction with other organisms within the marine ecosystem, and the potential risks to consumers. Author Contributions: L.S.S. conducted the research as part of her Doctorate degree in Environmen- tal Health. This study was supervised by J.F.R.L., I.S.H. and A.N.P. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the National Research Foundation (NRF), grant number— TTK190328424924. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: The data presented in this study are available on request from the corresponding author. Conflicts of Interest: The authors declare no conflict of interest. References 1. Chan, C.Y.; Tran, N.; Pethiyagoda, S.; Crissman, C.C.; Sulser, T.B.; Phillips, M.J. Prospects and challenges of fish for food security in Africa. Glob. Food Secur. 2019, 20, 17–25. [CrossRef] 2. Willer, D.F.; Aldridge, D.C. Microencapsulated diets to improve bivalve shellfish aquaculture for global food security. Glo. Food Secur. 2019, 23, 64–73. [CrossRef] 3. McLeod, C.; Polo, D.; Le Saux, J.C.; Le Guyader, F.S. Depuration and relaying: A review on potential removal of norovirus from oysters. Compr. Rev. Food Sci. Food Saf. 2017, 16, 692–706. [CrossRef] [PubMed] 4. 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[CrossRef] [PubMed] Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Journal
Aquaculture Journal – Multidisciplinary Digital Publishing Institute
Published: Apr 13, 2023
Keywords: shellfish; production areas; norovirus; hepatitis A; enteric viruses