Abstract
Pike is regularly consumed where it occurs and as a top predator in European water bodies especially prone to biomagnification of methylmercury. Therefore, upper limits for the mercury contamination of edible fish have been set in various food regulations. However, sold fish is rarely tested for its actual mercury contamination and despite fish meat considered safe according to food law, the amount of fish meat that could be eaten safely still remains unclear to consumers.
The aim of this review was to get an overview of mercury concentrations detected in the muscle flesh of pikes caught in European water bodies since the 1990s and derive dietary recommendations which would keep potential health impacts from mercury contaminants of consumed fish muscle flesh on an acceptable level.
Based on the reviewed studies the mercury concentrations in pike muscle flesh ranges from 70 – 2500 µg/kg wet weight, with length, body mass, age, and season of catchment of pikes as well as various water body characteristics being important factors associated with observed concentrations. From a nutritional perspective the reviewed studies indicate that on average a weekly intake of approximately 250g of pike flesh meat can be considered safe for an adult of 50 kg body weight. Susceptible subgroups like pregnant woman and women of childbearing age should avoid the consumption of pike muscle flesh completely or the most consume only half of this intake per week. Knowing the characteristics of a water body a pike originates from allows to reduce the likelihood of exceptional high mercury concentrations and therefore the potential for negative health impacts further. Among other environmental factors, water colour was identified as an important factor associated with pike mercury concentrations. Flesh of big pikes (>80 cm) from murky and warm (eutrophic) lakes should be prevented in dietary, whereas flesh meat of pikes from clear and cold water bodies with a length of ≤ 80 cm can generally be considered of higher quality in terms of potential mercury contamination.
Introduction
Besides being an excellent source of protein fish is rich in several other important nutrients, including polyunsaturated fatty acids, selenium, vitamin D, vitamin B-12, and niacin. On the other hand, regular consumption of fish such as pike (Esox Lucius, see Figure 1) can be a significant source of human mercury exposure. In fact, fish is known to account for most of the mercury intake by humans from daily food (Bloom, 1992; Lescord et al., 2018). This article focuses on pike (Esox lucius), a piscivore top predator in many lakes and rivers with opportunistic prey selection (Craig, 2008), which, where it occurs, is used as food and is of significance as a mercury source for humans (Kozak et al., 2023). However, even though, tolerable intake levels have been established for mercury by various health authorities, practical recommendations for consumers to determine the maximum intake while keeping the risk for negative health impacts on an acceptable level are often missing. The aim of this work is to derive dietary recommendations for pike muscle flesh based on a review of studies examining the mercury content in pike muscle flesh that were conducted in European water bodies after 1990.
Environmental impact and effects on human health
Mercury naturally occurs in the environment in low concentrations. However, the increased concentrations of environmental mercury since the industrial revolution is mainly associated with anthropogenic activities like mining, industrial manufacturing, agriculture and atmospheric deposition from burning of fossil fuels, especially coal (e.g. (Streets et al., 2017)). Most anthropogenic emissions consist of elemental mercury, which can be transported over long distances in the environment and deposited even in sparsely populated regions. Besides elemental mercury, mercury salts and organic mercury compounds occur in nature. The inorganic forms of mercury are predominant in the environment over the organic forms by several orders of magnitude. However, the biological impacts of mercury, are mainly associated with its organic forms, especially methylmercury, which is known to be the most toxic among the mercury compounds. It is known to be created when inorganic mercury circulating in the atmosphere is dissolved in aquatic systems. Over 95 % of the mercury contained in adult predatory fish muscle has been found to be methylmercury (Bloom, 1992; Lescord et al., 2018).
Most of the mercury released into the atmosphere ultimately settles in sediments of aquatic ecosystems, where it is transformed by microorganisms into methylmercury. In this form it is absorbed by phytoplankton, ingested by zooplankton and fish, leading to an up concentration in the food web, especially in long-lived predatory species at the top of the food chain such as pike. These processes called bioaccumulation and biomagnification, are the cause for the relatively high mercury concentrations in fish and past studies have regularly reported methylmercury concentrations in fish exceeding the recommended limits for human consumption (e.g. (Lavoie et al., 2013; Lindestrom, 2001)). As a consequence of bioaccumulation and biomagnification the mercury content in fish increases with age, weight and length (Zrnčić et al., 2013). Modifying factors for the uptake of mercury compounds from water include water pH and dissolved organic carbon content (Eisler, 2000). Since the 1980s, although fluctuations, have been reported, a general decreasing trend in fish mercury concentrations was observed (Braaten et al., 2014; Lodenius, 2015). This is due to the restrictions of use for mercury in industrial processes and due to the decrease of mercury emissions from European sources since the early 1990s (Lindestrom, 2001). For example, in a study conducted in finish water bodies, the average mercury concentration of a 1kg pike has decreased from 1.5 µg/g in the years 1971-74 to 0.8 µg/g in 1990 (Lindestrom, 2001).
With water concentrations of mercury as low as 0.015 µg/L an up-concentration in fish flesh of up to 1.47 µg/g has been reported in a study conducted in fathead minnow (Snarski & Olson, 1982). This means the concentration of mercury in fish can be almost 100,000-fold higher than in the surrounding water. Latest research further indicates that, future changes in climate and land use have the potential to raise the mercury concentration in fish further. Research conducted in lakes of Finnish Lapland found that the warmer and murkier a lake, the higher the mercury concentration in algae and this was reflected in fish species as well. Mercury concentrations in perch and pike living in warmer and eutrophic lakes was markedly increased compared to those living in pristine lakes (Ahonen et al., 2018; Kozak et al., 2021).
Regulatory environment and established limits
Because of its ecotoxicity and its risk to human health, upper limits for water mercury concentration as well as the mercury content of edible fish have been set in various recommendations and regulation. Moreover, in August 2017, the Minamata Convention on Mercury entered into force (Wang et al., 2019). It obligates the signed countries to control mercury emissions and the release of mercury to ambient air, water bodies and soil. It addresses several aspects necessary to reduce mercury use globally and to protect human health and the environment from the adverse effects of mercury.
For dietary exposure to methylmercury the Joint FAO/WHO Expert Committee on Food Additives (JECFA) established a tolerable intake of 1.6 µg/kg body weight per week in order to protect the developing fetus from neurotoxic effects (WHO, 2004). The JECFA further stated that life stages other than the embryo and fetus may be less sensitive to the adverse effects of methylmercury (WHO, 2007). For adults, up to about twice the tolerable intake per week (3.2 µg/kg body weight) would not pose any risk of neurotoxicity. Extrapolating this to an average adult with a body weight of 50 kg results in a safe weekly intake of fish meet if it does not contain more than 160 µg methylmercury. Health Canada, in contrast, established a maximum daily exposure level of mercury from all sources that was lowered in 1998 for women of child-bearing age and for children less than 10 years by 57% from 0.47 µg/kg/day down to 0.2 µg/kg/day (Jones, 1998). Extrapolating this to a weekly value gives a tolerable intake of 1.4 µg/kg body weight, which gives a maximum of 70 µg methylmercury within one week for the average adult with a body weight of 50 kg that can be safely in taken without negative health impacts.
The European directive on maximum levels for certain contaminants in food (EU 2023/915, 2023) and the directive on biota and surface waters (DIRECTIVE 2008/105/EC, 2008) took another approach to protect consumers and the environment and set an acceptable level of mercury in the muscle meat of fish, depending on the species of fish, of 500 and 1000 µg/kg, respectively, whereas directive 2008/105/EC set environmental quality standards (EQS) of 0.05 µg/L for surface waters and of 20 µg/kg for biota in general. Specifically for pike the acceptable limit of 1000 µg/kg for muscle meat is applicable. However, despite this limit being set, sold fish is rarely tested for its actual mercury contamination. Moreover, despite fish meat considered safe according to food law, the amount of fish meat that could be eaten safely remains unclear to consumers.
Results of reviewed environmental monitoring and studies
To ensure the safety of fish as a food source and to protect public health, regular monitoring of metal content in fish tissue is crucial (Çulha et al., 2016; Mehanna et al., 2016). Therefore, a comprehensive and continuous monitoring system is necessary to identify potential risks and ensure the safety of fish consumption. Such a monitoring program has been set up by the IKSR as one of the consequence of the Schweizerhalle disaster that occurred in an industrial area near Basel in 1986 (Giger, 2009). The incident resulted in a heavy contamination of the Rhine with various chemicals, amongst others, highly toxic mercury compounds. The latest published IKSR monitoring report which examined the contamination of fish in the aquatic system of the Rhine concludes that the environmental quality standard (EQS) of 20 µg/kg for mercury set for biota in Directive 2008/105/EG is systematically surpassed by fish examined in the course of the monitoring (IKSR Bericht Nr. 195, 2010). The report contrasted that the contamination of fish with mercury had to be considered problematic in terms of food law in some cases. It stated further, that mercury concentrations were mostly in the range between 70 and 350 µg/kg and the maximum levels for mercury under food law in accordance with EU Regulation 2023/915 were only exceeded in individual cases during the reporting period. However, the decline in mercury concentrations in Rhine fish observed in the 1980s and 1990s did not continue after 2000. Unfortunately, despite pike being sampled in the IKSR monitoring program, individual results for pikes were not reported and therefore the study has not been considered further in this review. Other studies examining mercury concentrations of pike in the Rhine were not found.
In Table 1 studies are listed which examined and reported mercury concentrations in pike muscle meat. The studies are ordered chronologically starting with the earliest study conducted in the Oder river from 1993-1994 and ending with the latest, which examined fish purchased from 2021–2022 at different points of sale all over Poland. The reviewed studies had a different basis for reporting the mercury content of pike muscle flesh. It was either reported as µg/kg wet weight (ww) or µg/kg dry weight (dw). As fish used for food is typically prepared on wet weight basis and also the acceptable limit for mercury in fish muscle meat according to EU food law is specified on a wet weight basis (EU 2023/915, 2023), highest reported dry weight values are extrapolated to wet weight basis applying a correction factor (CF). As water is the most abundant compound in muscle, ranging from 70 to 80% depending on the muscle, age at slaughter and animal species (Toldrá, 2003; van Ruth et al., 2014), the lower bound of this range has been used to derive a correction factor for the extrapolation of 0.3 (=(1-0.7)).
The earliest study conducted from June 1993 to October 1994 in the Oder river in Germany found mercury concentrations in the muscles of pikes, between 220 and 850 µg/kg, on a wet weight basis (Meinelt et al., 1997). The study from Enedina et al. conducted between December 2008 and September 2010 which examined seasonal variations of mercury concentrations in fish, reported the highest average mercury concentration and standard deviation for the month of December (Mean±sd 950±740 µg/kg ww), which indicates that highest mercury concentrations in pike are likely to be found after the end of the growing season (Enedina et al., 2014). In this study also a strong positive correlation between mercury concentration in the muscle tissue of pike and their length, body mass and age was noticed. Which is also highlighted by the fact that the highest value found in this study (2500 µg/kg ww) has been observed in the biggest and eldest individual of pike (112 cm, 9.8 kg and 16 years) examined.
Table 1: Studies after 1990 examining the mercury concentration in pike muscle flesh
Study details | Study results for pike muscle flesh (ww = wet weight; dw = dry weight) | Highest conc. (HC) reported (WCC) [µg/kg] | Margin of Safety of fish meat* (Accept. limit/HC) | Maximum safe intake of fish meat** (160 µg/HC) [g/week] |
Water body: River Oder, Germany; Year/Other: 1993-1994; 58 adult pike (37 females and 21 males with length ranging from 37 – 83 cm); Reference: (Meinelt et al., 1997) | 220 – 850 µg/kg ww | 850 = max | 1.17 | 188 g |
Water body: Lake Heddalsvatn, Norway Year/Other: Samples taken from pike and other fish in Dec. 2008, May 2010 and Sep. 2010 with length of pikes ranging from 25 – 112 cm and means of 51.7±16.7 cm (May), 39.9±14.5 cm (Sep), 63.3±24.4 cm (Dec); Reference: (Enedina et al., 2014) | May: 150 – 1300 µg/kg ww, (Mean±sd 640±330); Sep: 160 – 860 µg/kg ww, (Mean±sd 340±200); Dec: 70 – 2500 µg/kg ww, (Mean±sd 950±740); with highest value found in the biggest and eldest in- dividual of pike (112 cm, 9.8 kg and 16 years). | 2500 = max (from Dec.) | 0.40 | 64 g |
Water body: lakes of subarctic Tornio-Muoniojoki watercourse on the border of Sweden and Finland Year/Other: August–September 2009–2013; Reference: (Kozak et al., 2021) | Average adjusted total mercury content of pike from all lakes was 1209 µg/kg dw, with mean ± SD ranged from 890 ± 219 µg/kg dw in mesotrophic; 1126 ± 494 µg/kg dw in oligotrophic; 1658 ± 368 µg/kg dw in eutrophic lakes. | 608 = (mean + 1 x SD) x CF (from eutrophic lake) | 1.64 | 263 g |
Water body: Ten subarctic lakes of the Tornio-Muonio watercourse on the border of Sweden and Finland Year/Other: August–September (end of growing season) 2010–2013, ten pikes sampled from each lake; 86 pikes with 56.3 ± 17.0 cm, 1.269 ± 1.096 kg, 8.6 ± 3.6 years Reference: (Kozak et al., 2023) | eutrophic lakes: mean ± SD, 2236 ± 1262 µg/kg dw; colder oligotrophic lakes: mean ± SD, 1492 ± 1133 µg/kg dw; mesotrophic lakes: mean ± SD, 727 ± 332 µg/kg dw | 1049 = (mean + 1 x SD) x CF (from eutrophic lake) | 0.95 | 152 g |
Water body: Lakes of Warmia and Mazury Region, Poland; Year/Other: October 2013; with pike lengths ranging from approx. 50 – 75 cm; Reference: (Łuczynska & Paszczyk, 2019) | mercury content in muscles of pike was found to be (mean ± SD): 297 ± 111 µg/kg ww, | 408 = mean + 1 x SD | 2.45 | 392 g |
Water body: Study examined fish for human consumption Year/Other: Fish including pike were purchased in 2021–2022 at different points of sale all over Poland; Reference: (Brodziak-Dopierała & Fischer, 2023) | Reported result for pike: mean mercury concentration of 128 µg/kg ww (SD and range not reported) | 128 = mean | 7.8 | 1250 g |
*The margin of safety (MOS) has been calculated for pike muscle meat with the environmental quality standards (EQS) specified in the EU directive 2023/915 applied as the acceptable limit (1000 µg/kg). If the resulting MOS is ≥ 1 the examined fish meet can be considered safe according to EU food law, whereas values <1 indicate fish meet that can considered as problematic according to EU food law. **Based on the tolerable intake of 3.2 µg/kg body weight derived by JECFA extrapolated to an average adult with 50kg body weight, which results in a safe weekly intake of fish meet if it does not contain more than 160 µg methylmercury.
The study from Kozac et al conducted between August–September 2009–2013 in lakes of the subarctic Tornio-Muoniojoki watercourse on the border of Sweden and Finland assessed the impact of biological factors on mercury biomagnification (Kozak et al., 2021). It found the highest average mercury concentration in muscle meat for pikes caught in eutrophic lakes (mean ± SD: 1658 ± 368 µg/kg dw). Adjusting this to wet weight basis with the CF derived above gives an average concentration of 498 µg/kg with a standard deviation of 110 µg/kg. The study from Kozak published in 2023 examined pikes from ten lakes in the same region and sampled 10 pike from each lake at the end of the growing season (August-September) between 2010 and 2013 (Kozak et al., 2023). In this study the highest average mercury concentration in muscle meat for pikes caught was also observed in eutrophic lakes with mean ± SD = 2236 ± 1262 µg/kg dw, which corresponds to mean ± SD = 670 ± 379 µg/kg on a wet weight basis. The study conducted by Łuczynska & Paszczyk in October 2013 tested pikes from lakes of the Warmia and Mazury region in Poland and detected an average mercury content in muscles of pike on wet weight basis of 297 µg/kg with a standard deviation of 111 µg/kg (Łuczynska & Paszczyk, 2019). Brodziak-dopierała et al. examined fish for human consumption that were purchased from 2021–2022 at different points of sale all over Poland (Brodziak-Dopierała & Fischer, 2023) and reported a mean mercury concentration for pike muscle meat of 128 µg/kg wet weight.
Discussion
Except for some pikes from the study of Lake Heddalsvatn in Norway (Enedina et al., 2014) and some pikes from eutrophic lakes of the Tornio-Muonio watercourse on the border of Sweden and Finland (Kozak et al., 2023), the muscle meet of all examined pikes can be considered safe for human consumption in terms of the environmental quality standards (EQS) specified in European food law (EU 2023/915, 2023). The studies with exceptions are indicated by an MOS <1 in Table 1. However, the study from Kozac et al. published in 2023 is only marginally below, due to the big pike from the eutrophic lake. All pikes from this study that were sampled from mesotrophic and oligotrophic lakes have an MOS > 1 when the highest reported concentration is adjusted to wet weight basis. Similarly, all pikes sampled from the study conduct in Norway in May have an MOS < 1.
Table 2: Observed range of mercury concentration in pike muscle flesh adjusted to wet weight basis
| Study | Reported or estimated range of mercury concentration [min – max]* |
| (Meinelt et al., 1997) | 220 – 850 µg/kg |
| (Enedina et al., 2014) | 70 – 2500 µg/kg |
| (Kozak et al., 2021) | 190 – 608 µg/kg |
| (Kozak et al., 2023) | 108 – 788 µg/kg |
| (Łuczynska & Paszczyk, 2019) | 186 – 408 µg/kg |
| (Brodziak-Dopierała & Fischer, 2023) | 128 µg/kg |
*When individual values for min and max measurements were not reported, the min was estimated as mean – SD and the max value as mean + SD and if values were reported in dry weight both values were adjusted to wet weight using the derived correction factor (0.3). For the study conducted by Brodziak-dopierała only the mean value was reported, therefore the range could not be estimated.
Based on the reported and estimated mercury concentration ranges (see Table 2) the highest variance in detected muscle flesh mercury concentrations was observed in the study conducted by Enedina et al in Norway at lake Heddalsvatn, with detected mercury concentrations ranging from 70 µg/kg to 2500 µg/kg.
In comparison with the other studies the broad range in the Enedina et al. study is most likely due to the high dispersion in the length of pikes that have been tested, and the positive correlations between mercury concentration in muscle tissue of fish and their length, body mass and age, that has been confirmed in various studies (Enedina et al., 2014; Rask et al., 2024; Zrnčić et al., 2013). The maximum mercury concentration found in this study (2500 µg/kg ww) has been observed in the biggest and eldest individual of pike (112 cm, 9.8 kg and 16 years) examined. Studies that examined a narrower range of pike lengths such as the studies from Meinelt et al. (37 – 83 cm) and Łuczynska & Paszczyk (approx. 50 – 75 cm), reported also significantly lower highest concentrations of 850 µg/kg wet weight and 408 µg/kg wet weight, respectively.
In a review similar to this, specifically done for the Pannonian and Romanian section of the Danube river, a significantly lower maximum concentration was found in pike muscle meat, with reported mercury concentration ranging from 0.021 – 0.428 µg/kg (Cordeli et al., 2023). However, similar to our review the authors recognized age of the fish and test location as important factors influencing the mercury contamination of fish muscle flesh.
Applying the tolerable intake of 3.2 µg/kg body weight derived by JECFA, weekly maximum safe intake values for pike muscle flesh have been derived based on the highest reported concentrations in studies (see Table 1). In this manner safe intakes of 64 – 1250 g/week were obtained for an adult of 50 kg. Excluding the Enedina et al study that contained the exceptionally big pike and the study from Brodziak-Dopierała & Fischer which only reported a mean value for the amount of mercury detected in pike muscle meat, results in an average safe intake across studies of 249 g/week. Hence, from a nutritional perspective, the reviewed studies indicate that on average a weekly intake of approximately 250g of pike flesh meat can be considered safe for the average adult (50kg body weight) when applying the tolerable intake of 3.2 µg/kg body weight derived by JECFA. In order to minimize the risk of developmental neurotoxic effects to an acceptable level, susceptible subgroups like pregnant woman and women of childbearing age should avoid the consumption of pike muscle flesh completely or the most consume only half of this intake per week. The reviewed studies indicated further, that knowing the characteristics of a water body a pike originates from allows to reduce the likelihood of exceptional high mercury concentrations and therefore the potential for negative health impacts further. Among other environmental factors, water colour was recognized as an important factor associated with pike mercury concentrations, in a study conducted between 1983 and 2013 in lakes located in the Evo forest area of southern Finland (Rask et al., 2024). In this study highest pike mercury concentrations were recorded in 2002 after consistent browning of the lakes, suggesting a dominant role of dissolved organic carbon (DOC) in the lake water mercury dynamics. Based on this finding and the observations of the other studies discussed above, it can be concluded that flesh of big pikes (>80 cm) from murky and warm (eutrophic) lakes should be prevented in dietary, whereas flesh meat of pikes from clear and cold water bodies with a length of ≤ 80 cm can generally be considered of higher quality in terms of potential mercury contamination.