Unguryanu Et Al 2022 Human Health Risk Assessment of Heavy Metals From Meat and Offal of Reindeer and Cow in The Far
Unguryanu Et Al 2022 Human Health Risk Assessment of Heavy Metals From Meat and Offal of Reindeer and Cow in The Far
Unguryanu Et Al 2022 Human Health Risk Assessment of Heavy Metals From Meat and Offal of Reindeer and Cow in The Far
research-article2022
SJP0010.1177/14034948221096243T. N. Unguryanu et al.Heavy metals in meat and risk assessment
Human health risk assessment of heavy metals from meat and offal of
reindeer and cow in the Far North of European Russia
1Department of Hygiene and Medical Ecology, Northern State Medical University, Russian Federation, 2Higher School of
Natural Sciences and Technologies, Lomonosov Northern (Arctic) Federal University, Russian Federation, 3F. Erismann
Institute of Public Health, Sechenov First Moscow State Medical University (Sechenov University), Russian Federation
Abstract
Aims: This study aimed to compare the concentrations of heavy metals in reindeer and cow meat and offal originating from
the Nenets Autonomous Okrug, Northwestern Russia, and to assess the risk to the health of the indigenous population
associated with heavy metal intake due to the consumption of reindeer and cow. Methods: Lead, cadmium, mercury, and arsenic
concentrations were measured in 39 muscle, 15 liver, and 14 kidney samples from reindeer and 33, 18, and 12 corresponding
samples from cow in 2014–2016 using atomic absorption spectrometry. Estimated daily intake of investigated heavy metals,
hazard quotient, hazard index and cancer risk were calculated. Results: Mean cadmium and mercury concentrations in reindeer
liver and kidney exceeded the maximum permissible levels for bovine animals. However, the estimated daily intakes of heavy
metals through consumption of reindeer and cow meat and offal were lower than tolerable daily intakes. Hazard quotient and
hazard index values for heavy metals in reindeer and cow samples were <1. Hazard index values were in descending order:
reindeer kidney (0.389)>reindeer muscle (0.382)>cow muscle (0.088)>reindeer liver (0.051)>cow kidney (0.012)>cow
liver (0.004). The cancer risk related to the consumption of reindeer and cow meat and offal did not exceed acceptable
levels. Conclusions: There is no human health risk associated with heavy metal intake due to the consumption of
reindeer and cow meat and offal originating from the Nenets Autonomous Okrug.
Keywords: Heavy metals, risk assessment, reindeer meat, cow meat, liver, kidney
Correspondence: Tatiana N. Unguryanu, Northern State Medical University, Troitsky Ave 51, Arkhangelsk 163000, Russian Federation.
E-mail: [email protected]
© Author(s) 2022
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1010 T. N. Unguryanu et al.
developmental abnormalities, hematologic and immu- absorption spectrometry with flame atomization was
nologic disorders, and various types of cancer, and applied for the determination of Pb and Cd [12], with
they may have adverse effects on the blood, central hydride atomization for the determination of As [13].
nervous system, and kidneys [7]. Cd and As are classi- Hg was determined using atomic absorption spec-
fied as human carcinogens, and Pb as probably carci- trometry of “cold vapor” [14]. Concentrations of
nogenic to humans, according to the International heavy metals are stated in milligrams per kilogram
Agency for Research on Cancer [8]. wet weight (mg/kg w/w).
Reindeer Cow
Muscle (n=39) Liver (n=15) Kidney (n=14) Muscle (n=33) Liver (n=18) Kidney (n=12)
Pb Geom. mean 0.028 0.250a,b 0.121c 0.023 0.031d 0.026d
95% CI 0.020–0.038 0.204–0.309 0.097–0.149 0.018–0.029 0.021–0.044 0.023–0.029
90th Percentile 0.092 0.429 0.178 0.043 0.062 0.034
Range 0.005–0.120 0.160–0.450 0.070–0.180 0.010–0.054 0.013–0.062 0.021–0.035
Cd Geom. mean 0.008 0.470a,b 1.640c 0.006 0.041d 0.136d
95% CI 0.006–0.009 0.372–0.594 1.024–2.632 0.004–0.008 0.033–0.044 0.123–0.151
90th Percentile 0.022 0.814 3.689 0.013 0.049 0.162
Range 0.005–0.028 0.230–0.830 0.500–3.890 0.005–0.014 0.032–0.051 0.111–0.162
Hg Geom. mean 0.006 0.183a,b 0.648c 0.003d <LOD <LOD
95% CI 0.005–0.008 0.143–0.235 0.542–0.774 0.002–0.005
90th Percentile 0.021 0.284 0.920 0.008
Range 0.003–0.070 0.072–0.314 0.380–0.920 0.002–0.008
As Geom. mean 0.006 0.014a 0.014c 0.007 <LOD <LOD
95% CI 0.005–0.007 0.008–0.023 0.012–0.016 0.005–0.008
90th Percentile 0.014 0.030 0.019 0.013
Range 0.005–0.025 0.001–0.030 0.011–0.020 0.005–0.013
As: arsenic; Cd: cadmium; CI: confidence interval; geom.: geometric; Hg: mercury; LOD: limit of detection; Pb: lead.
aIndicates significant difference between reindeer muscle and liver; bindicates significant difference between reindeer liver and kidney; cindicates significant
difference between reindeer muscle and kidney; dindicates significant difference between reindeer and cow.
concentration in reindeer liver (0.183 mg/kg) and assessed based on the HQ. Although individual HQs
kidney (0.648 mg/kg) exceeded the MPL in Russia for each metal were below unity, particular attention
by 1.8 and 3.2 times, respectively. The mean con- should be paid to some high individual HQ values.
centration of Hg in reindeer muscle was 2.0 times The highest HQ values were found for Cd and Hg in
higher than that in cow muscle (p=0.023). In addi- reindeer kidney (0.196 and 0.186 respectively) and
tion, the highest mean concentrations of Hg were for As and Hg in reindeer muscle (0.137).
observed in reindeer liver and kidney, and these Considering that all heavy metals were found in
exceeded the concentration in reindeer muscle by meat and offal samples and were consumed simulta-
31 and 108 times, respectively (p<0.001). neously, the HI was also calculated (Figure 1). The HI
As was found in 27% and 38% of reindeer and values for all analyzed heavy metals followed the
cow muscle samples and 100% of all reindeer offal descending order of: reindeer kidney>reindeer
samples, As content was lower than LOD in all cow muscle>cow muscle>reindeer liver>cow kidney>cow
offal samples. The As content of all samples did not liver. The maximum HI was observed in reindeer kid-
exceed the MPLs set by TR CU 021/2011 (0.1 mg/ ney and muscle (0.389 and 0.382 respectively),
kg in muscle, 1.0 mg/kg in liver and kidney) [24]. whereas cow kidney and liver showed the minimum
Generally, As content in reindeer offal was two HI (0.012 and 0.004 respectively). For reindeer and
times higher than in muscle (p<0.001). Reindeer cow meat and offal, the HI values were less than unity,
and cow muscle had equal concentrations of As thereby indicating negligible potential risk to human
(p=0.557). health. CR values for Pb, Cd, As, and TCR did not
exceed the acceptable values (Table III).
Human health risk assessment
RFDILs
The calculated EDIs of Pb, Cd, Hg, and As by the
NAO indigenous population through the consump- Based on the concentrations of all investigated heavy
tion of reindeer and cow meat and offal were lower metals, consumption of local cow muscle and liver
than the TDIs recommended by the FAO/WHO does not need to be restricted (more than 500 g/day/
JECFA [18,19]. The highest EDIs of Pb (0.191 μg/ person can be eaten), whereas the RFDIL for cow
kg, bw/day) and Cd (0.196 μg/kg, bw/day) were kidney is only 370 g/day (Table IV). The RFDIL for
through the consumption of reindeer muscle and reindeer muscle is 490 g/day, while that for reindeer
reindeer kidney, respectively (Table II). liver is 70 g/day. The greatest restriction is applied to
The non-carcinogenic health effects of meat and reindeer kidney (15 g/day) due to a high concentra-
offal consumption from the two animal species were tion of Cd.
Heavy metals in meat and risk assessment 1013
Table II. Estimated daily intakes (EDIs) of heavy metals (μg/kg-day) and hazard quotients (HQs).
EDIs HQs
Pb Cd Hg As Pb Cd Hg As
Reindeer muscle 0.191 0.055 0.041 0.041 0.053 0.055 0.137 0.137
Reindeer liver 0.021 0.039 0.015 0.001 0.006 0.039 0.051 0.004
Reindeer kidney 0.011 0.196 0.056 0.001 0.003 0.196 0.186 0.004
Cow muscle 0.087 0.023 0.011 0.026 0.024 0.023 0.038 0.088
Cow liver 0.003 0.003 – – 0.001 0.003 – –
Cow kidney 0.002 0.011 – – 0.001 0.011 – –
0.40
0.35
0.30
0.25
Hazard Index
0.20
0.15
0.10
0.05
0.00
Reindeer Reindeer Cow muscle Reindeer liver Cow kidney Cow liver
kidney muscle
Pb Cd Hg As
Figure 1. Hazard indices and relative contributions of single heavy metals through consumption of meat and offal of reindeer and cow.
Table III. Carcinogenic risk of lead (Pb), cadmium (Cd), and and kidney exceed the MPL for bovine animals.
arsenic (As).
However, the EDIs of heavy metals for the NAO
Pb Cd As TCR indigenous population through consumption of rein-
Reindeer muscle 1.63 E-6 2.08 E-5 6.15 E-5 8.39 E-5
deer and cow meat and offal were lower than the
Reindeer liver 1.77 E-7 1.49 E-5 1.75 E-6 1.68 E-5 TDIs. The HQs for studied heavy metals in all rein-
Reindeer kidney 9.21 E-8 7.44 E-5 1.63 E-6 7.61 E-5 deer and cow tissues were <1. The HI values of all
Cow muscle 7.04 E-7 8.63 E-6 3.97 E-5 4.91 E-5 heavy metals were below unity and followed the
Cow liver 2.20 E-8 1.30 E-6 – 1.32 E-6
Cow kidney 1.84 E-8 4.31 E-6 – 4.33 E-6
descending order of: reindeer kidney>reindeer
muscle>cow muscle>reindeer liver>cow kidney>
TCR: total cancer risk. cow liver. Individual CR and TCR via consumption
of reindeer and cow meat and offal did not exceed
Discussion acceptable values (between 1×10-4 and 1×10-6).
The elevated heavy metal concentrations in rein-
The present study has shown that concentrations of deer offal, as compared with those in cow offal, may
the analyzed heavy metals varied between species of be explained by dietary habits. Cow diet predomi-
bovine animals and tissue types. The heavy metal con- nantly consists of grasses, but reindeer feed mainly
centrations in reindeer offal were significantly higher on lichens. In northern regions, lichens represent
than those in cow offal. Reindeer kidney had the high- between 50–77% of the reindeer diet during the fall
est concentrations of Cd and Hg, but the highest con- and winter seasons [26]. Lichens are long-lived,
centration of Pb was observed in reindeer liver. The receive nutrients and water via precipitation, and can
mean concentrations of Cd and Hg in reindeer liver accumulate contaminants from the ground and from
1014 T. N. Unguryanu et al.
Table IV. Calculated recommended food daily intake limits for times lower than that in Greenland (0.7–1.0 kg/week
meat and offal consumption by the Nenets Autonomous Okrug or 100–142 g/day) [30]. Differences in the recom-
population (g/person/day).
mended maximum intake of reindeer tissues across
Pb Cd Hg As All heavy metals circumpolar regions suggest that regular control of
Reindeer muscle NL NL 490 NL 490 heavy metal concentrations is important to develop
Reindeer liver 480 70 110 NL 70 realistic recommendations concerning local reindeer
Reindeer kidney NL 15 40 NL 15 consumption.
Cow muscle NL NL NL NL NL
Cow liver NL NL – – NL
One limitation of the present study is that the
Cow kidney NL 370 – – 370 data on meat and offal consumption were obtained
from other studies carried out in the NAO [11], the
As: arsenic; Cd: cadmium; Hg: mercury; NL: no limitation (>500 g/day/ neighboring Yamalo-Nenets Autonomous Okrug
person); Pb: lead.
[17], and from the annual surveys of food con-
sumption conducted by Rosstat [16]. Using this
the air, while grasses are less influenced by atmos- data, the EDIs could only be calculated for average
pheric deposition [27]. Reindeer and caribou from consumption of meat and offal by the indigenous
lichen-rich areas, compared to those from areas with- population. Future dietary surveys should be car-
out lichens, have a higher level of toxic elements [28]. ried out using a food frequency questionnaire to
Ingestion of soil may also be a route of reindeer/cari- determine the frequency and amount of meat and
bou tissue contamination [29]. offal from reindeer, cattle, and other domestic ani-
Based on the measured concentrations of the stud- mals consumed in different ages, sexes (children,
ied heavy metals and TDI limits, we could infer that adult men and women, pregnant/lactating women),
the consumption of reindeer meat and offal is not and populations (indigenous and non-indigenous)
associated with any health risk for the indigenous in the NAO. These data are necessary to assess the
population of the NAO in spite of the fact that the human health risk of exposure scenarios of central
concentrations of Cd and Hg in reindeer liver and tendency and high-end consumption of meat and
kidney exceeded MPLs. Low human exposure to Pb, offal in different population groups.
Cd, and Hg through consumption of reindeer meat
and other edible reindeer tissues was demonstrated in
Mid- and Northern Norway, although the Cd level Conclusion
exceeded the MPL for bovine animals by 52% in The level of contamination of reindeer tissues was
reindeer liver samples [6,26]. A study from Yukon, higher than that of cow tissues. Reindeer liver and
Canada showed that the risk of Hg exposure from kidney had the highest concentrations of heavy met-
caribou consumption is low, as HQs were <1 [5]. als. The mean concentrations of Cd and Hg in rein-
However, Makarov et al. [29] investigated contamina- deer liver and kidney exceeded the MPLs for bovine
tion of reindeer meat and offal in the Russian Far animals. The EDIs of heavy metals for the NAO
North and reported that the consumption of reindeer indigenous population through consumption of rein-
kidney by populations in the Murmansk Region, the deer and cow meat and offal were lower than the
Yamalo-Nenets Autonomous Okrug, Kamchatka, TDIs. There is no human health risk associated with
Chukotka, Karelia, and Yakutia may result in a Cd the studied heavy metals due to consumption of rein-
intake that exceeds the TDI by more than three times. deer and cow meat and offal originating from the
Taking into account levels of reindeer tissue con- NAO.
tamination in the NAO, the calculated RFDILs for
reindeer muscle, liver, and kidney are 490 g/day, 70 Acknowledgements
g/day, and 15 g/day respectively. These recommended
consumption levels of reindeer meat and offal for the The authors wish to thank the State Regional Center
NAO are lower than for Chukotka, where consump- for Standardization, Metrology and Testing in the
tion of reindeer meat is unrestricted, and the recom- Arkhangelsk Region and the Nenets Autonomous
mended maximum intake of reindeer liver and kidney Okrug, Russia for data on heavy metal concentrations
is 100 g/day [3,23]. The calculated RFDIL for rein- in meat and offal samples from reindeer and cow.
deer kidney from the NAO is comparable with the
maximum recommended weekly intake of caribou Declaration of conflicting interests
kidney from Greenland (0.132−0.164 kg/week or The author(s) declared no potential conflicts of
18–23 g/day) due to Cd contamination, but the rec- interest with respect to the research, authorship, and/
ommended liver intake in the NAO is almost two or publication of this article.
Heavy metals in meat and risk assessment 1015
Funding absorption spectrometry method after pressure digestion. GOST R
53183-2008. Moscow: State Committee of the Russian Feder-
The author(s) received no financial support for the ation for Standardization, Metrology and Certification, 2009.
research, authorship, and/or publication of this article. [15] Risk-assessment guidance for superfund. Human health evaluation
manual. Part A. Interim report (final). Report No.: EPA/540/1-
89/002. Washington, DC, USA: Office of Emergency and
ORCID iD Remedial Response, U.S. Environmental Protection Agency,
1989.
Tatiana N. Unguryanu https://orcid.org/0000- [16] Household food consumption in 2018. Statistical handbook.
0001-8936-7324 Moscow: Russian Federal State Statistics Service, 2019.
[17] Agbalyan E and Listishenko A. About toxic and carcino-
genic risks for population in the Yamalo-Nenets Autono-
References mous Okrug. In: Gorbanev SA and Frolova NM (eds)
[1] Arctic Monitoring and Assessment Programme (AMAP). Problems of maintaining health and ensuring sanitary and
AMAP Assessment 2009: Human health in the Arctic. Oslo, epidemiological welfare of population in the Arctic. Saint-
Norway: AMAP, 2009. Petersburg, Russia: OOO “IPK “Kosta” 2017. pp.14-20
[2] Gibson J, Adlard B, Olafsdottir K, et al. Levels and trends [in Russian].
of contaminants in humans of the Arctic. Int J Circumpolar [18] World Health Organization (WHO). Evaluation of certain
Health 2016;75:33804. contaminants in food: Seventy-second report of the Joint FAO/
[3] Dudarev A. Dietary exposure to persistent organic pollut- WHO Expert Committee on Food Additives. WHO TRS 959-
ants and metals among Inuit and Chukchi in Russian Arctic JECFA 72. WHO: Geneva, Switzerland, 2011.
Chukotka. Int J Circumpolar Health 2012;71:18592. [19] World Health Organization (WHO). Evaluation of certain
[4] Shepeleva O, Novikova Y and Degteva G. Food safety in contaminants in food: Seventy-third report of the Joint FAO/
Arctic and Subarctic territories of the Russian European WHO Expert Committee on Food Additives. WHO TRS 960-
North. Ekologiya cheloveka [Human ecology]. 2019;10:24- JECFA 73. WHO: Geneva, Switzerland, 2011.
32 [in Russian]. [20] United States Environmental Protection Agency. Integrated
[5] Schuster R, Gamberg M, Dickson C, et al. Assessing risk of Risk Information System, https://www.epa.gov/iris (2017,
mercury exposure and nutritional benefits of consumption accessed 15 June 2021).
of caribou (Rangifer tarandus) in the Vuntut Gwitchin First [21] Federal contaminated site risk assessment in Canada. Part
Nation community of Old Crow, Yukon, Canada. Environ II: Health Canada Toxicological Reference Values (TRVs).
Res 2011;111:881-887. In: Environmental Health Assessment Services, Safe Environ-
[6] Hassan A, Brustad M and Sandanger T. Concentrations and ments Programme. Health Canada: Ottawa, ON, Canada,
geographical variations of selected toxic elements in meat 2004, pp.1-2.
from semi-domesticated reindeer (Rangifer tarandus tarandus [22] California Office of Environmental Health Hazard Assess-
L.) In mid- and northern Norway: Evaluation of risk assess- ment. CompTox Chemicals Dashboard, https://comptox.epa.
ment. Int J Environ Res Public Health 2012;9:1699-1714. gov/dashboard/chemical-lists/OEHHA (2020, accessed 10
[7] Tchounwou P,Yedjou C, Patlolla A, et al. Heavy metal toxic- May 2021)
ity and the environment. Exp Suppl 2012;101:133-164. [23] Dudarev A, Yamin-Pasternak S, et al. Traditional diet and
[8] International Agency for Research on Cancer. Agents classi- environmental contaminants in Coastal Chukotka IV: Rec-
fied by the IARC monographs, volumes 1–125. Lyon, France: ommended intake criteria. Int J Environ Res Public Health
International Agency for Research on Cancer, 2020. 2019;16:696-710.
[9] Population distribution of the Arkhangelsk region by sex [24] Custom Union’s technical regulations on food safety requirements.
and age on 1 January 2020. Statistical Handbook. Arkhan- TR CU 021/2011, Commission of the Customs Union. 2011.
gelsk: Arkhangelskstat, 2020. [25] European Commission. Commission regulation (EC) no
[10] All-Russian population census in 2010. Moscow: Russian Fed- 1881/2006 of 19 December 2006 setting maximum levels
eral State Statistics Service, 2011. for certain contaminants in foodstuffs. Official Journal of the
[11] Dallmann W, Peskov V and Murashko O. Monitoring of devel- European Union, 2006;364:5-24.
opment of traditional indigenous land use areas in the Nenets [26] Hassan A, Rylander C, Brustad M, et al. Level of selected
Autonomous Okrug, NW Russia. Norwegian Polar Institute: toxic elements in meat, liver, tallow and bone marrow of
Tromsø, Norway, 2010. young semi-domesticated reindeer (Rangifer tarandus taran-
[12] State Committee of the Russian Federation for Standard- dus L.) From Northern Norway. Int J Circumpolar Health
ization, Metrology and Certification. Raw material and 2012;71:1-7.
food-stuffs. Atomic absorption method for determination of toxic [27] Garty J. Biomonitoring atmospheric heavy metals with
elements. GOST 30178-96. Moscow: State Committee of lichens: Theory and application. CRC Crit Rev Plant Sci
the Russian Federation for Standardization, Metrology and 2001;20:309-371.
Certification, 1997. [28] Aastrup P, Riget F, Dietz R, et al. Lead, zinc, cadmium, mer-
[13] State Committee of the Russian Federation for Standard- cury, selenium and copper in Greenland caribou and rein-
ization, Metrology and Certification. Raw material and food- deer (Rangifer tarandus). Sci Total Environ 2000;245:149-159.
stuffs. Atomic absorption method for determination of arsenic. [29] Makarov D, Komarov A, Ovcharenko V, et al. Dioxin and
GOST R 51766-2001. Moscow: State Committee of the heavy metals contamination of reindeer offal from Russian
Russian Federation for Standardization, Metrology and far North regions. Sel’skokhozyaistvennaya biologiya [Agri-
Certification, 2002. cultural biology]. 2018;53:364-373 [in Russian].
[14] State Committee of the Russian Federation for Standardiza- [30] Gamberg M, Cuyler C and Wang X. Contaminants in two
tion, Metrology and Certification. Foodstuffs. Determination West Greenland caribou populations. Sci Total Environ
of trace elements. Determination of mercury by cold-vapor atomic 2016;554-555:329-336.