Monitoring programme for veterinary control on seafood products imported to Norway from third countries – results from 2018

As a member of the European Economic Area (EEA), Norway is obliged to monitor the conformity of products imported to the EEA area. As part of this activity, analytical examinations of seafood with respect to microorganisms, parasites and the presence of undesirable substances are conducted. The Norwegian Food Safety Authority (NFSA) is the competent authority regarding veterinary border control in Norway. On behalf of NFSA, IMR have carried out the analytical examination of the seafood samples in this monitoring programme and elaborated this report.

According to Commission Regulation (EC) No 136/2004 (EU, 2004; FOR-2015-11-30-1347) the monitoring plans must be based upon the nature of the products and the potential risks associated with the different product categories, concidering all relevant factors such as frequency and number of incoming consignments and results from previous monitoring. The selection of parameters included in the current analytical activity was based on previous findings in this program, as well as information available in the RASFF, “Rapid Alert System for Food and Feed” system of the European commission.

The spectrum of products examined by NFSA at veterinary border inspection points is large, as it reflects the annual flux and variation in the import activity. Thus, the methods used to examine the products are also diverse.

Microbiological parameters are used to evaluate the quality of seafood products and if proper hygienic measures were applied during production. To evaluate possible fecal contamination, analysis for common indicator organisms were conducted, including assays for coliforms, bacteria in the Enterobacteriaceae family and enterococci. Furthermore, samples were analyzed for specific pathogens relevant for food safety, including bacteria in the geni Salmonella, Listeria and Vibrio. EU microbiological criteria, which Norway has implemented through the EEA agreement, have been established for Salmonella and Listeria monocytogenes (Commission Regulation 2073/2005). In addition, analysis for H₂S-producing bacteria in unpreserved and non-heat treated seafood was implemented, in order to provide information on the quality of fresh and frozen seafood, as well as hygienic standards during production.

The survey included the chemical spoilage indicators histamine and total volatile basic nitogen (TVN).

Parasites are common in commercially harvested seafood species. Parasites potentially have a negative human health impact and they can reduce the aesthetical appearance of the product. However, in seafood only a few widely distributed parasite species are of consumer health concern. The larvae of several species of roundworms (nematodes) commonly occur in commercially harvested marine fish stocks in temperate sea areas worldwide. In addition to the quality reducing effect of these parasites, they are of human health concern when found alive in undercooked, lightly brined, marinated or raw fish meat products. According to Regulation (EC) No 853/2004, fishery products intended to be consumed raw or almost raw should undergo a freezing treatment to kill viable parasites. This regulation does not apply to farmed fish when the absence of such parasites has been well documented (Commission Regulation 1276/2011). Accordingly, the number of nematodes only was determined in relevant products.

According to current EU legislation (Directive 96/23), some drugs are illegal to use in animals intended for food production. Thus, samples from aquaculture were analyzed for such agents. Chloramphenicol is an antibiotic agent with activity against a broad spectrum of microorganisms. Due to a rare but serious dose-independent adverse effect (aplastic anaemia), this agent is not authorized in the treatment of food-producing animals, including fish. Nitrofuranes were previously widely used in veterinary medicine as an antimicrobial agent. They were banned from use in the European Union (EU) in 1995 due to concerns about the carcinogenicity of their residues in edible tissue. Relevant farmaceuticals were analysed in farmed seafood products.

Persistent organic pollutants (POPs) form a heterogeneous group of lipophilic substances that exhibit a range of chemical and toxicological characteristics. They are persistent in the environment and accumulate in food chains. Some clases of POPs are considered a dietary hazard to human health. The compliance of selected samples with the established maximum levels for food stuffs (EC 1881/2006) was evaluated for the contaminats: dioxins, furans, and dioxin-like PCBs, the EU selected “non-dioxin like-PCBs”, and for the polyaromatic hydrocarbons (PAH). Chlorinated pesticides and flame-retardant compounds in the polybrominated diphenyl ethers family (PBDEs) were also measured. However, maximum limits have not been established for these.

Undesirable trace elements relevant for seafood safety occur naturally in the environment with large geographical variations, due to their geological presence. Furthermore, they are released from anthropogenic sources. These compounds may to some extent accumulate in food chains and thus find their way into wild caught seafood. Cultured seafood can be affected via contaminated feed. As implemented in regulation EC 1881/2006, the elements cadmium (Cd), mercury (Hg), and lead (Pb), were measured and the compliance of the values with the maximum levels was evaluated. Arsenic (As) was also measured, although no maximum limit for As in seafood exists and only a minor fraction of the here measured total arsenic is present in the toxic inorganic form in seafood.

Sampling was carried out by NFSA at the Norwegian Border Inspection Posts (BIPs) while analytical examinations and the writing of this report was conducted by IMR. The sampling targeted hazards associated with each kind of imported products, and took into account import volumes, compositional nature of the products, results from previous monitoring, geographical origin of samples, and information available in the Rapid Alert System for Food and Feed (RASFF). This report concerns samples imported to Norway in 2018.

Fresh sample were directly shipped to IMR and frozen samples were stored frozen in the BIPs until shipment in the frozen state to IMR for analysis. Upon arrival, samples were registered at the IMR sample reception unit, each sample photographed, and relevant information registered in a Laboratory Information Management System (LIMS). The microbiological assay was carried out prior to all other sample handling. The sample was then further prepared for analyses and split in sub-samples (aliquots) for the different assays and analytical methods.

In general, the edible part of the samples for human consumption was selected for analyses, according to a manual with specific instructions for each kind of sample. For species where a legal maximum level was defined, the tissue specified in the regulation was selected. The analytical methods and procedures used were accredited according to the ISO 17025 standard, unless otherwise specified. A summary of the chemical analytical methods, accreditation status and their performance data are listed in Annex 2.

The evaluations of the analytical data in the report is based primarily on the EU maximum levels (Commission Regulation (EU) No. 2006/1881, summed up in Annex 3 of this report; Commission Regulation (EU) No. 2073/2005, 37/2010 and 1019/2013) and EU recommendations. The maximum levels provide a legal framework for trade. For undesirables with no maximum level in place, the reference basis selected for the discussion/ interpretation was published opinions or food safety evaluation from scientific expert committees (when available), or the analytical range commonly observed for this undesirable in seafood from pristine or semi-pristine waters.

A total of 122 samples from the NFSA at Norwegian BIPs, were examined by a selection of methods for microorganisms, parasites and undesirable chemical species as shown in the table below. Data tables are presented in Annex 1. Method performance data are listed in Annex 2. A summary of EU maximum levels for certain contaminants in foodstuffs are listed in Annex 3.

3.1 - Microbiology

The detailed results from the microbiological examinations are listed in Annex 1 (Table 1). A total of 104 samples were examined for microorganisms by a range of assays.

Incubation test and plate count for nine canned seafood products showed that these products were sterile.

Fifty samples were analysed for the presence of quality reducing H₂S-producing seafood spoiling bacteria. Of these, five samples had 1000 or more cfu/g. These samples included three samples of Yellowfin tuna, two from Sri Lanka and one from the Maldives. The two remaining samples were one sample of Yellowtail from Australia, and one sample of Eastern oysters from Canada.

One sample of Eastern Oysters from Canada was examined for E. coli by the Donovan method as specified by EU, and < 18 bacteria/100 gram sample material was found (result not shown in table).

Fifty-nine samples were analysed for coliforms by the 3M TM Petrifilm method, and numbers above the detection level of 10 cfu/g were found in two samples. One sample of Yellowfin tuna imported from the Maldives had counts of 310 coliforms/g, and a sample of Pacific cod fillet imported from Thailand had 60 coliforms/g. The same two samples also showed high counts of thermotolerant coliform bacteria (560 and 60 cfu/g respectively). All results for the determination of thermotolerant coliforms by the 3M TM Petrifilm method (94 samples in total), except the two samples mentioned, were below the detection limit of 10 cfu/g.

Twenty-five samples were analysed for the presence of coagulase positive Staphylococcus, and all were under the levels of detection (100 cfu/g). Thirty samples were analysed for the presence of anaerobic sulphite-reducing bacteria, and one sample of shrimp imported from Canada had counts of 1000 cfu/g. Bacteria in the family Enterobacteriaceae were under the detection limit in the nine samples examined, except one sample of feed imported from Chile which contained 10 cfu/g.

Sixty samples were analysed for the presence of enterococci, and two samples had 100 cfu/g, which is the detection limit. These were one sample of Yellowfin tuna from Vietnam, and one of Pacific cod from Thailand.

Fifty-seven samples were analysed for L. monocytogenes and the bacterium was detected qualitatively in one sample of Pacific cod from Thailand, and in one sample of Atlantic herring from Norway. The sample of Pacific cod was further examined quantitatively, and the number of L. monocytogenes was found to be below the detection limit of 10 cfu/g. The sample of Norwegian herring was exported to Egypt but rejected due to limited storage space at the arrival destination, and was subsequently returned to Norway where it was examined.

No pathogens in the genus Salmonella (n=95 samples) were detected. Vibrio sp. was qualitatively detected in two of twenty-one analysed samples, one of whole, headless scampi from Vietnam, and one sample of peeled, headless scampi from India. The strains isolated from these two samples were sent to NMBU in Oslo for further characterisation and identified as V. cholerae and V. parahaemolyticus respectively. The V. cholerae isolate did not possess cholera toxin producing genes.

The presence of yeast and moulds were examined in ten samples. Yeast was detected in four samples, in two samples of feed from Chile (2000 and 18000 cfu/g), in one sample of dried Yellow Stripe Trevally from Thailand (1400 cfu/g), and in Migas from China (400 cfu/g). Mould was detected in two samples, the same dried Yellow Stripe Trevally from Thailand (2200 cfu/g), and in Migas from China (100 cfu/g) as the yeast was detected in (not shown in table).

3.2 - Parasites

Parasitological examinations were carried out on Forty fish samples, some of which were processed seafood products (Table 2). Nematodes were found in nine of them (22.5%). The fish were imported frozen; hence the nematodes were dead and not infective at the time of analysis. However, allergic symptoms may be triggered in sensitive individuals from dead as well as live nematodes. The highest numbers of nematodes (21), were found in a sample of Atlantic cod (Gadus morhua) imported from the Russian federation.

3.3 - Drug residues and dyes

Thirteen samples originating from aquaculture were analysed for residues of prohibited veterinary medicines (unauthorised dyes and antibacterial agents) in 2018. The analysis included the dye compounds crystal violet (CV), leuco crystal violet (LCV), malachite green (MG), leuco malachite green (LMG), brilliant green (BG), and the antibacterial agents chloramphenicol and nitrofuran metabolites. None unauthorised dyes were detected in any of the analysed samples, nor were any traces of chloramphenicol or nitrofuranes found. Details of analysed samples are given in Table 3 (unauthorised dyes) and Table 4 (antibacterial agents).

3.4 - Chemical spoilage indicators

The chemical spoilage indicator histamine and total volatile basic nitrogen (TVBN)was examined in a total of twenty-nine samples, with nineteen samples analysed for each of them (Table 5). All results were compliant. The two highest histamine values of 20 and 30 mg/kg ww were found in samples of Peruvian anchovy (Engraulis ringens). The highest TVBN value of 32.8 mg/100g ww, was found in a sample of Yellowfin tuna (Thunnus albacares).

3.5 - Undesirable trace elements

The concentrations of the elements arsenic (As), cadmium (Cd), lead (Pb) and mercury (Hg) were examined in 89 samples, selected by criteria intended to maximize the probability of finding non-compliant concentrations. The analytical data are listed in Table 6.

In seafood, arsenic is mainly present as organo-metal chemical species of low toxicity, such as arsenobetaine and arsenolipids. This characteristic of marine foods set them apart from foods of terrestrial origin, in which toxic inorganic arsenic species give a significant contribution to the elemental arsenic concentration. Thus, no relevant maximum level on elemental As was in place for the samples analysed. The observed values for elemental As were mostly within the range occasionally observed in seafood from pristine waters. However, two samples of Pandalus shrimp from the Russian Federation, were measured with relatively high concentrations of 140 and 170 mg/kg ww.

A sample of canned sardine in oil, Sardinella longiceps, from the Philippines, exhibited a Cd value of 0.1 mg/kg ww. This value is assumed to be above its maximum level considering that the analysed food sample had been processed. The listed NHC samples (not intended for human consumption), values were measured up to 0.7 mg/kg ww. The seafood maximum limit does not apply. For a basis of value interpretation: the highest maximum level for elemental Cd in food is 1.0 mg/kg ww (in kidney of bovine animals.)

A significant part of the elemental Hg in seafood is present in the organic form of methylmercury, a compound with a documented toxic character. Thus, there are maximum levels in place for elemental Hg in seafood, but not specifically for the methylmercury species (EU, 2006) (Annex 3). However, all methylmercury  is measured as part of the total elemental mercury concentration. A frozen fillet sample of Yellowfin tuna Thunnus albacares imported from Vietnam exceeded the maximum Hg level of 1.0 mg/kg ww with a measured value of 1.5 mg/kg ww.

For lead, one sample of small crabs from Thailand (Sesarma mederi), was measured to 0.69 mg/kg ww. The maximum level applies to “muscle meat from the limbs and abdomen” or to whole animals if the are intended to be eaten whole (EU,2006, footnote 25), which we assumed for this sample. Thus, the whole crabs were analysed. The measured value was then slightly above the maximum level.

3.6 - Persistent organic pollutants (POPs)

A selection of the most relevant samples were analysed for dioxins (PCDDs), furans (PCDFs) dioxin-like PCBs (DL-PCBs), non-dioxin-like PCBs (NDL-PCBs), also referred to as: EU-PCB6 or “indicator” PCBs. Also included were polybrominated flame-retardants (PBDEs), chlorinated pesticides and PAHs. Annex 3 provides a summary of the most relevant maximum levels.

3.6.1 - Dioxins (PCDDs), furans (PCDFs) and Polychlorinated Bifenyls (PCBs)

Table 7 lists the sum values of PCB, dioxins and furans, in terms of the summed dioxin like PCBs (DL-PCBs), the summed non-dioxin-like PCBs (NDL-PCBs), and the summed PCDDs and PCDFs, for each of the analysed samples. The maximum levels are defined in terms of upper bound sum-parameters (EU, 2006, footnote 32; EU, 2011) except for the sum-parameter NDL-PCBs which is the summed analytical values in the ng/g w.w. scale. The other sum-parameters are measured in the TEQ pg/g w.w. scale (toxic equivalents): in effect summing toxicities rather than their analytical concentrations, as specified in the regulation (EC) 1881/2006 (EU, 2006).

One Atlantic cod liver sample stood out with high values of sum DL-PCBs compared to the listed fillet values. However, the value was compliant to the fish liver maximum level. One sample of fish oil from Turkey, 2018-539/1 was measured to 2.6 and 7.4 pg/g ww (TEQ), UB LOQ for the sum of PCDD/DFs and for the total sum of dioxins and DL-PCBs respectively. These values are non-compliant regarding the maximum levels.

3.6.2 - Polybrominated diphenyl ethers (PBDEs or BDEs)

BDEs are flame-retardant compounds found in plastics, textiles, electronic castings and circuitry. As these products age and eventually are discarded, the PBDEs finds their way into the environment and from there, into biota and into food and feed. The EU recommends a monitoring of the BDE compound class in food (EU, 2014). However, no maximum limits have been established in food. EFSA performed a risk assessment of BDEs in food in 2011 (EFSA CONTAM Panel, 2011). They concluded that the current dietary exposures of BDE-47, -153 and -209 did not raise health concerns. However, the current dietary exposure of BDE-99 was labelled a potential health concern. The data for individual BDE congeners (BDE-28, 47, 99, 100, 153, 154 and 183) and their upper bound sum (BDE7) for the twenty-eight samples are listed in Table 8. All the measured values were within a range occasionally observed in seafood from pristine waters.

3.6.3 - Organochlorine pesticides

Organochlorine pesticides are legacy compounds, previously used for pest control in agriculture. A number of these compounds have for years been banned from use by international treaties. Due to a history of extensive use, they are characterised by a ubiquitous presence in the environment and in food chains. Presently, low levels of these compounds still find their way into the human diet. Concentration of concern may be found in samples from local hot spots, reflecting historical contamination: These compounds are also found in freshwater species, reflecting a history of agricultural impact.

No less then thirty organochlorine pesticides compounds (listed in Annex 2 together with their corresponding LOQ) were measured in fifteen samples. Most of these compounds could not be quantified (all values < LOQ) in any sample. The values for compounds found in quantity (value > LOQ) in two or more of the samples are listed in Table 9a and 9b. The highest values were found for compounds in the DDT family, with a maximum of 13 ng/g ww for p,p'-DDT, and 12 ng/g ww for beta-HCH (hexachloro-hexane), both found in the same anchoveta oil from China.

3.6.4 - Polyaromatic hydrocarbons (PAH)

PAH-compounds are generated from incomplete combustion of organic matter. In food processing PAHs may be formed from over-heating, and they find their way into smoked products from the smoking process. Bivalves can be contaminated from environmental PAH pollution adsorbed to water-suspended particles when these are ingested by the bivalve. There is a high number of compounds in this class. A few of them exhibit food safety issues: Maximum levels are in place for bivalves and smoked products (Annex 3); for Benzo(a)pyrene (BaP) alone, as well as for the lower bound sum (LB-sum) (EU, 2006) of four selected PAH compounds; BaP, Benzo(a) anthracene, Benzo(b)fluoranthene and chrysene (LB-sum PAH₄).

Only one sample was selected for PAH analysis, a smoked mackerel sample. Twenty individual PAH compounds were measured. Only the PAH data associated with a maximum level are listed. In this sample the measured values were below the limit of detection, and thus below the maximum levels.

In total 122 samples, collected by the official staff at the Norwegian Border Inspection Posts of the Norwegian Food Safety Authority, were examined for selected chemical, microbiological and/or parasitological undesirables in 2018.

The results for microbiological quality parameters and indicator organisms for faecal contamination generally showed low numbers in the 104 examined samples. However, higher counts were found in some samples. One sample of Yellowfin tuna imported from the Maldives had 310 coliforms/g and 560 thermotolerant coliform/g, and one sample of Pacific cod imported from Thailand had 60 coliforms/g and 60 thermotolerant coliform/g.

Further, five samples had 1000 or higher cfu/g of quality reducing H₂S-producing seafood spoiling bacteria. These samples included three samples of Yellowfin tuna, two from Sri Lanka and one from the Maldives, as well as one sample of Yellowtail from Australia, and one sample of Eastern oysters from Canada.

L. monocytogenes was detected qualitatively in one sample of Pacific cod from Thailand, however, further quantitative examination showed that the number of bacteria was below the detection limit of 10 cfu/g. L. monocytogenes was also detected in one sample of Norwegian herring exported to Egypt and re-imported to Norway. No samples had pathogens in the genera Salmonella. Enterobacteriaceae was detected in one sample of feed imported from Chile.

Ten samples were examined for the presence of yeast and moulds. Their presence was detected in four and two samples respectively. Yeast was found in two samples of feed from Chile (2000 and 18000 cfu/g), in one sample of dried Yellow Stripe Trevally from Thailand (1400 cfu/g), and in Migas from China (400 cfu/g). Mould was detected in the same dried Yellow Stripe Trevally from Thailand (2200 cfu/g), and in Migas from China (100 cfu/g) as the yeast was detected in.

Parasitological examinations were carried out on Forty fish samples. Nematodes were found in nine of them (22.5%). The fish were frozen when imported. Hence the nematodes were dead and not infective at the time of analysis. However, also dead nematodes can trigger allergic symptoms in sensitive individuals.

Thirteen samples, originating from global aquaculture were examined for residues of selected prohibited pharmaceuticals. The examination included the dye compounds crystal violet, leuco crystal violet, malachite green, leuco malachite green and brilliant green. And also chloramphenicol and nitrofuran metabolites. No unauthorised dyes, nor residues of prohibited antibacterial agents were detected.

The chemical spoilage indicators were examined in twenty-nine samples. All results were compliant with their maximum levels.

The undesirable trace elements arsenic, cadmium, mercury and lead, were measured in 89 samples. With respect to cadmium, a sample of canned sardine in oil from the Philippines exhibited a value of 0.1 mg/kg ww, which is above its maximum level. One sample of small crabs from Thailand should be noted: Assuming the crabs were intended to be consumed whole, the measured lead concentration was slightly above their maximum level. A frozen fillet sample of yellowfin tuna imported from Vietnam with a value of 1.5 mg/kg ww exceeded the maximum mercury level. There is no maximum level for for arsenic in seafood, reflecting the low toxicity of its marine chemical molecular species. The measured elemental arsenic values were within a range commonly observed in seafood.

Concerning the Chlorinated POP compounds, twenty-eight samples were analysed for dioxins and furans, for PCBs, including the twelve dioxin like PCBs, the six EU selected non-dioxin like PCBs, and seven polybrominated diphenyl ethers. One sample of fish oil from Turkey was non-compliant with its maximum levels. The remaining values were within the ranges commonly found in seafood.

Fifteen samples were analysed for organochlorine pesticides. A majority of the 30 different pesticides could not be detected or quantified in any of the samples. The highest quantifiable values were found for some compounds in the DDT family, and for beta-HCH, both with a maximum in an anchoveta oil imported from China.

Regarding PAHs, One sample was analysed in 2018. It was compliant with its maximum levels.

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