Dietary composition in Greenland 2000, plasma fatty acids and persistent organic pollutants

Science of the Total Environment 331 (2004) 177–188

Dietary composition in Greenland 2000, plasma fatty acids and persistent organic pollutants Bente Deutcha,*, Henning Sloth Pedersena,b, Jens C. Hansena a

Centre of Arctic Environmental Medicine, Aarhus University, Vennelyst Boulevard 6, DK 8000, Aarhus, Denmark b Primary Health Care Center, Nuuk, Greenland Accepted 1 March 2004

Abstract Human exposure to pollution in the Arctic presents a potential future health risk for the local populations. Epidemiological studies in Greenland have shown that human blood levels of several organic contaminants are very high, especially in the North where people depend on local food. In East Greenland (Ittoqqortoormiit (Scoresbysund)) the population shows the highest blood levels of several persistent organic pollutants found in Arctic countries, especially PCB, the levels of which exceed Canadian guideline levels. As in other Arctic countries, the direct source of these contaminants is the diet, and it is, therefore important to monitor the composition of the diet along with other factors which may influence the metabolism and thereby the accumulation of toxic substances. This project is part of the human health program of the ongoing circumpolar ‘Arctic Monitoring and Assessment Programme’. Dietary survey results (Semiquantitative Food Frequency questionnaire from 192 men and women from East Greenland and 48 men from Uummannaq West Greenland) were analysed along with other factors (lifestyle and anthropometric factors), blood lipids, fatty acid profiles, and concentrations of persistent organic pollutants (POPs). The dietary survey showed that the contributions of traditional food provided 25–30% of the total energy intake. However, the relative monthly meal intake of seal, whale, polar bear, fish and game, and the composition of imported food, varied between districts. The blood fatty acids (FA), e.g. the n-3yn-6 ratio (Uummannaq 0.70, Ittoqqortoormiit 0.37 Tassiilaq 0.45) showed moderate associations with the overall reported food composition. The n-3 fatty acids were associated with the well-known lowering effect on serum-triglyceride levels. The strongest associations between diet and plasma fatty acids were found for docosapentaenoic acid, C: 22.5.3 which strongly correlated with reported seal, and polar bear intake (Ps0.01** and 0.04*, respectively), consistent with the fact that seal and polar bear blubber contain much higher concentrations of C: 22.5.3 than other sea mammals and fish. Seal and polar bear intake, and in particular all the plasma n-3 fatty acids, were significantly correlated with organic contaminant concentrations, (betaHCH, chlordanes, DDTs, Hexachlorobenzene, Mirex, PCBs, and toxaphenes) P-0.01**. Conclusions: The strongest correlations between POPs and fatty acids were found with C: 22.5.3, strongly indicating seal and polar bear blubber as the main contributors of POPs to the local population. 䊚 2004 Elsevier B.V. All rights reserved. Keywords: Greenland; Diet; Fatty acids; Organic pollutants

*Corresponding author. Tel.: q45-8942-6172; fax: q45-8942-6199. E-mail address: [email protected] (B. Deutch). 0048-9697/04/$ - see front matter 䊚 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2004.03.028

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1. Introduction Epidemiological studies in Greenland have shown that human blood levels of various anthropogenic contaminants are very high (AMAP, 1998). In East Greenland (Ittoqqortoormiit (Scoresbysund)) the population shows the highest blood levels of several persistent organic pollutants found in Arctic countries especially PCB (Deutch and Hansen, 2000). As in other Arctic countries the direct source of these contaminants is the diet, and it is, therefore important to monitor the diet and other factors, which may influence metabolism. The diets of Arctic Indigenous Peoples consist of both traditional food and imported (market) foods. Although it varies by country, locality, sex and age group the traditional food yields 10–40% of the total energy intake and this percentage has decreased over the last 30–40 years (Deutch, 2002). In Greenland, recent dietary surveys have shown that the relative intake of traditional food is 25– 30% by weight (Pars, 2000; Deutch, 2002, 2003). The traditional foods are the main contributors of protein, fat, and most minerals (Fe, Zn, Se, I), vitamin D, and especially of the essential long chain n-3 fatty acids, which in several ways can be considered as health promoting. The high relative content of n-3 fatty acids in the traditionalycountry foods presumably provides some protection against cardiovascular diseases, and various other diseases of an affluent industrialized society (Jul et al., 1994). However, human blood levels of marine n-3 fatty acids are strongly associated with blood levels of persistent organic pollutants (POPs), because the main sources of POPs are fats (blubber) from marine animals. Thus the traditional food is the main contributor of persistent organic pollutants, particularly if the content of marine fish and mammals is high (Bjerregaard et al., 2001). The correlation between the intake of traditional food items as determined by dietary surveys, and blood levels of anthropogenic substances, have been demonstrated on both a group and a population basis for heavy metals (Hansen, 1990) and for organochlorines (Van Oostdam et al., 1999).

Chemical analyses of food items of animal origin have provided ample proof that traditional food is a major source of heavy metals (Hg, Cd and some times Pb) and persistent organic substances (Johansen et al., 2000, 2002). Furthermore, since the POPs are biomagnified through the food chain, the animals at higher trophic levels have, in general, higher blood levels of organic contaminants, although size and age also have an influence. Exposure estimates for heavy metals calculated from dietary intake data show good correlations with human tissue concentrations (Hansen and Pedersen, 1986; Hansen, 1990). Dietary exposure estimates of persistent organic pollutants (POP) have, so far, only been compared with human body burdens of POPs on a population basis, and no correlations between estimates of individual dietary intakes and individual blood levels of organic xenobiotics have previously been available. However, several studies have shown very significant positive associations between n-3 fatty acids in human lipid fractions and blood levels of both Hg (Hansen and Pedersen, 1986; Dewailly et al., 2001) and POPs (Deutch and Hansen, 2000) which makes the connection between intake of marine mammal fat (e.g. blubber) and organic pollutants highly probable. The present study will assess the associations between self reported dietary food frequencies for indigenous peoples in East Greenland (ns192) and Uummannaq, West Greenland (ns48) and the levels of plasma phospholipid fatty acids (FA), and a number of lipophilic persistent organic pollutants, including 10 pesticides, 14 PCB congeners, five Toxaphenes. In particular it will focus on the long chain n-3 fatty acids, namely the eicosapentaenoic acid, EPA (C20.5.3), docosapentaenoic acid, DPA (C22.5.3) and docosahexaenoic acid DHA, (C22.6.3) both individually and using their mutual ratios as markers of subsistence marine animals. 2. Materials and methods The proposed protocols of the studies were accepted by the Ethical Committee for Scientific Investigations in Greenland and all the participants gave written informed consent. This project is part

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Table 1 Demographic, anthropometric, and lifestyle factors in Greenland (1999–2000) according to self reported AMAP questionnaire

Total n Age Height, cm Weight, kg Body mass index, BMI Danish meals

a

Inuit mealsa Meals per month with birds Fish Game Lamb Polar bear Seal Whale

Uummannaq

Ittoqqortoormiit

Tasiilaq

48 men 38.1: (28–54) 170 (158–181) 74.4 (60–91) 25.6 (21–33) 9.4 (1–28) 17.3 (8–28) 1.9 (1–8) 7.1 (1–20) 1.2 (0–9) 3.4 (0–20) –not askedb

52 men and 42 women 32.8: (18–45) 166 (149–190) 74.6 (42–160) 27.2 (19–64) 15.9 (1–28) 8.9 (1–28) 1.6 (0–20) 2.1 (0–20) 2.7 (1–28) 0.8 (0–2) 3.1 (1–30) 3.1 (1–8) 1.1 (0–8)

40 men and 48 women 31.6: (19–45) 163 (146–181) 69.6 (39–97) 26.0 (17–40) 14.5 (1–28) 8.6 (1–28) 1.2 (0–8) 4.9 (0–28) 0.5 (0–1) 1.0 (0–8) 1.5 (1–12) 5.5 (1–28) 1.4 (0–8)

11.7 (2–28) 2.6 (0–20)

Arithmetic means and (ranges). None of the values listed differ significantly between men and women. a Danish meals or Inuit meals were asked as separate questions. Thus ‘Inuit meals’ is not just the sum of the meals containing various local food items since ‘a meal ‘ may contain more than one type of local food b Polar bear is not normally consumed in the Uummannaq district.

of the human health program of the ongoing circumpolar ‘Arctic Monitoring and Assessment Programme’. Dietary survey results from a Semiquantitative Food Frequency questionnaire (35 local and 25 Danish food items, eight frequency categories) are presented from 192 men and women from East Greenland and 48 men from Uummannaq West Greenland. The results have been sampled and analysed along with other factors included in the questionnaire (lifestyle and antropometric factors), blood lipids, fatty acid profiles, and persistent organic pollutants (POPs). The participants were randomly drawn from the public register and were all of Inuit decent, defined as having more than two grandparents born in Greenland. In Uummannaq, 14 non-smokers

selected separately were also included (Deutch et al., 2003). All respondents completed the standard questionnaire developed by the Danish National Institute of Public Health for the Arctic Monitoring and Assessment programme, AMAP. It included questions about demographic and lifestyle parameters (e.g. current and previous smoking levels, drinking habits) and a simple questionnaire with 14 food items and six frequency categories. In addition, the participants were also asked separate questions about the monthly number of Danish or Inuit meals. Since a meal may contain more than one type of local food, Inuit meals are not the sum of reported single local food items, Table 1. In addition, the participants answered a more detailed semiquantitative food frequency question-

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naire, FFQ (adapted from Willet, 1998) which consisted of 60 food items, namely 35 local Greenland food products, mainly local fish, mammals, birds, and local berries and 25 Danish imported food types, mainly meat products, grain, bread, milk products, fruit and vegetables. There were 10 frequency categories ranging from once a year to several times a day, and all categories were used. Standard (and not individually reported) portion sizes were used to estimate daily intakes in grams of food and the relative weights of Danish and local food in the diet. Blood samples were taken for the determination of plasma organochlorine concentrations (microgram per litre and microgram per kg lipid), cholesterol, triglycerides, phopholipids, total lipids (gy l and mmolyl), and fatty acid profiles (distribution in % of phospholipid fatty acids). The blood samples were frozen at y20 8C and transported to Queen Ingrids Hospital, Nuuk. Here they were stored at y80 8C until further transport. The plasma samples were analyzed at a certified laboratory, Le Centre de Toxichologie, Sainte Foy, Quebec, Canada (AMAP, 1998) for 11 pesticides, 14 PCB-congeners (CB28, CB 52, CB99, CB101, CB105, CB118, CB128, CB138, CB153, CB156, CB170, CB180, CB183, CB187) and four toxaphenes of which only two congeners, parlar numbers 26 and 50, were above the detection limits of the analysis. For simplification and comparison with international data, some group-variables were used in the presentation of results, namely, the sum of chlordanes, the sum of DDE and DDT, the sum of 14 CB congeners, the sum of toxaphene congeners and with the sum of the 3HCH isomers, hexachlorobenzene and mirex. To minimize the effects of possible daily variations in plasma fatty acids, the fatty acid profiles were determined in plasma phospholipids (at the Biology Department, University of Guelph, Canada) (Deutch et al., 2003). Since previous studies have shown a linkage between smoking and high POP blood levels (Deutch and Hansen, 2000; Deutch et al., 2003) smoking was controlled for in the multivariate statistical analysis and the plasma-cotinine concentration was used as an indicator of nicotine breakdown products and current smoking status or

exposure. Cotinine (ngyl) was determined at Unit of Experimental Biology, Department of Environmental and Occupational Medicine, University of Aarhus Denmark (Deutch et al., 2003). All the data were analyzed using SPSS-statistics program versions 9.0 and 10.0. Descriptive univariate analysis was performed on all parameters included in the study. Bivariate correlation analyses were carried out between questionnaire answers and analytical results. The arithmetic means of log-transformed contaminant concentrations were calculated and compared by Independent samples, t-test. Geometric means, medians and ranges are given in Deutch (2002, 2003). Multiple linear regression analyses were performed for a number of plausible models, and model control was performed for the best models. Significance levels were P-0.05*, P-0.01**, P-0.001***. In the final linear regression analyses logarithmic concentrations of POPs were used so as to approximate normal distributions. In bivariate correlation analyses, Spearman coefficients were used. The current project was funded by the Danish Environmental Protection Agency as part of the environmental support program Dancea-Danish Cooperation for Environment in the Arctic. The authors are solely responsible for all results and conclusions presented in the report and they do not necessarily reflect the opinions of the Danish Environmental Protection Agency. 3. Results The participant profile is shown in Table 1. The average age of particpants was slightly higher in Uummanaq, but the anthropometric factors were very similar in the three towns. wThe average height was 170 cm for men and 159 for women, average BMI (body mass index: kg per square meter) was 26.0 for men and, 25.1 (in Tasiilaq) and 26.7 (in Ittoqqortoormiit) for women.x Except for weight and height which varied between men and women, the large majority of the lifestyle factors and blood levels of lipids and contaminants did not vary significantly between men and women, which have, therefore been combined. However, since the participants from Uummannaq included 14 non-smokers, this group could not be

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considered totally representative for the area. This could potentially influence both the anthropometric and dietary factors, but the dietary factors did not, in fact, differ significantly between smokers and non-smokers. There were also a higher number of hunters in Uummannaq with a more marine based diet and this shows up in the dietary composition. The general dietary habits investigated in a small 14 item (AMAP) questionnaire show that the intake frequency of seal, fish and whale was higher amongst participants from Ummannaq than on the East coast, Table 1. The reported number of ‘Inuit meals’ and ‘Danish meals’ should, in principle, add up to approximately 30 per month but the sums turn out to be a little lower, which probably reflects a small inconsistency in the answers. As mentioned above, since a meal may contain more than one type of local food, ‘Inuit meals’ are not the sum of reported single local food items but usually lower (Table 1). The results of the dietary surveys as shown by semiquantitative FFQ, which covered the previous year, were, in general, very similar between Ittoqqortoormiit and Tasiilaq, and the mean and median intakes were almost identical with only a few exceptions. The total intakes of local Greenland products were the same but the total intake of Danish products was higher (though not significantly) in Tasiilaq. The resulting relative solid weight intake of local products was 31.3% in Ittoqqortoormiit and 24.8% in Tasiilaq. Amongst the Greenland products, the intakes of polar bear, walrus and game (muskox, reindeer, hare) were significantly higher in Ittoqqortoormiit whereas intakes of seal and fish products were higher (though not significantly) in Tassilaq. Amongst the Danish products, meat and bread intakes were the same in both towns, but milk products, fruit and vegetable intakes were higher in Tasiilaq. The liquid intake was the same in both towns, as was sugar intake, which followed coffee and tea drinking. In general, the diet was more varied in Tasiilaq for both local and Danish products. In Ummanaq the total intake of local products was 28%, and was relatively similar to Tassilaq, except for a higher intake of seal and whale and no polar bear intake.

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Of all the local food items, seal was the most common and was eaten in all three districts and by practically all participants at least once or twice a month throughout the year. Fish was the second most common food item consumed and is available all year in Tasiilaq and Uummannaq, but not in Ittoqqortoormiit. The intake of whale meat was more sporadic, reflecting variable hunting seasons. The food intakes of men and women were compared for each town and found to be very similar, deviating only for fruit (Ps0.02) and vegetables (Ps0.07) intakes of which were higher amongst women. The participants were also analyzed as two age groups wbelow and above 32 years (the median age)x but there were no significant differences in food consumption within the age range tested (20– 50 years) and no clear relationship with age. The diets of smokers and non-smokers were compared, but there were no significant differences in dietary pattern. The results of the dietary survey are presented in more detail elsewhere (Deutch, 2003). The plasma fatty acids and other lipids (Table 2) reflected the same overall picture. However, although the total intake of traditional food was higher in Ittoqortoormiit, the intake of local marine products was the lowest, due to a very low fish intake in the diet, n-3yn-6s0.37. The marine food intake was higher in Tassilaq and highest in Uummannaq, with the n-3yn-6 ratios equalling, 0.45 and 0.70, respectively. Both triglyceride and cholesterol levels were significantly lower in Uummannaq, Table 2, and triglycerides were inversely correlated with the n-3yn-6 ratio (Spearman rsy 0.23, P-0.001). Thus the n-3 fatty acids were associated with the well-known lowering effect on serum-triglycerides. All the n-3 fatty acids were mutually correlated at high significance levels and of course they were also all significantly correlated with the n-3yn-6 ratio. Therefore any correlation found with any one of these fatty acids would also apply to all the others. The blood levels of lipophilic organic contaminants are presented in Table 3 on a lipid basis; see also Deutch (2003) for further detail. This table shows that, overall, concentrations of contaminants in blood followed the same pattern as the dietary markers of marine food intake shown in Table 2.

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Table 2 Arithmetic means and (S.D.) of total plasma lipids, triglycerides, cholesterol and fatty acids (% of plasma phospholipids) in Greenland 1999–2000

Total n Total lipids, gyl Triglycerides mmolyl Cholesterol mmolyl Linolic acid, C18.2.6 Arachidonic acid C20.4.6 Eicosapentaenoic acid C 20.5.3 Docosapentaenoic acid, C22.5.3 Docosahexaenoic acid, C 22.6.3 Sum n-3 Sum n-6 n-3yn-6

Uummannaq (a)

Ittoqqortoormiit (b)

Tasiilaq (c)

48 men 6.27 (1.17) ab** 1.18 (0.86) ab*

52 men and 42 women 7.07 (1.26) bc ns 1.55 (0.84) bc ns

40 men and 48 women 7.26 (1.50) ac*** 1.66 (0.81) ac**

5.08 (0.79) ab**

5.57 (1.02) bc ns

5.85 (1.25) ac**

14.25 (4.09) ab***

19.22 (3.86) bc ns

19.16 (3.39) ac***

4.68 (0.98) ab***

5.79 (1.10) bc***

4.81 (0.92) ac ns

5.48 (3.44) ab***

2.64 (2.01) bc*

3.40 (2.22) ac***

1.42 (0.37) ab 0.07 ns

1.29 (0.44) bc ns

1.21 (0.31) ac ***

5.89 (1.35) ab**

5.05 (1.68) bc***

5.91 ( 1.58) ac ns

13.42 (4.62) ab*** 21.46 (4.50) ab*** 0.70 (0.40) ab***

9.60 (3.70) bc*** 28.11 (4.11) bc** 0.37 (0.21) bc**

11.20 (3.71) ac** 26.50 (3.87) ac*** 0.45 (0.21) ac***

Compared between districts by independent samples t-test. The values do not differ significantly between men and women. Uummannaq vs. Ittoqqortoormiit (ab), Uummannaq vs. Tasiilaq (ac), Ittoqqortoormiit vs. Tasiilaq (bc). P-0.05*, P-0.01**, P-0.001***, nssnon-significant.

However, there were specific differences between compounds. The sum of chlordanes, DDE, hexaclorobenzene, mirex and toxaphenes were significantly higher in Uummannaq than on the east coast. The concentrations of CBs were extremely high in Ittoqqortoormiit, and the levels of beta HCH were high in both Ittoqqortoormiit and Uummannaq. Concentrations of all the POPs were significantly lower in Tasiilaq than in the two other locations (Table 3). This difference in distribution shows that the external sources of POPs may vary from place to place. This could result from differences in dietary composition as well as from different contaminant levels in subsistence animals. In addition both the DDT concentration and the DDTyDDE ratio (not shown) was higher amongst men in Ittoqqortoormiit than in the other districts. This points to a more recent local exposure to DDT, which may not be from a dietary source. Associations (Spearman’s bivariate correlations) are presented in Table 4 between the monthly meal intakes of seal, polar bear, whale, and fish products derived from the food frequency questionnaire and

plasma levels of n-3 fatty acids. Data for the three districts are presented separately. This table shows that the reported seal intake was significantly correlated with all the plasma n-3 FA in all three districts. Polar bear intake was significantly correlated with DPA and DHA but not with EPA. Whale intake was significantly correlated with DPA and n-3yn-6, and (borderline significance) with DHA in Uummannaq, and fish intake was significantly correlated with DHA and borderline with EPA and n-3yn-6, also only in Uummannaq. Thus DPA was significantly correlated with more marine food items than the other n-3 fatty acids. It also shows a possible association between food intake and the overall plasma POPs levels (signifying five or more of the eight investigated POP types), see also Table 5. Table 5 shows the associations between reported meal frequencies in East Greenland and the lipid adjusted POP levels in plasma. The calculations were performed for the two towns both independently and taken together. Since it has been found in several studies that smoking influences the

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Table 3 Geometric means of organochlorine (POPs) blood levels (microgramykg lipid) from three districts in Greenland (1999–2000) and significance levels in independent samples t-test of logn transformed variables Lipid adjusted POPs

Uummannaq (a)

Ittoqqortoormiit (b)

Tasiilaq (c)

Beta HCH Sum of chlordanes DDE Hexaclorobenzene Mirex Sum of PCB Sum of Toxaphenes

71.1 ab ns 1759 ab*** 1920 ab*** 496 ab*** 88.1 ab** 2871 ab** 344 ab***

73.6 bc *** 892 bc*** 1408 bc** 194 bc*** 53.9 bc** 4287 bc*** 144 bc ns

22.7 ac*** 489 ac*** 1023 ac*** 118 ac*** 34.1 ac*** 1527 ac*** 129 ac***

Uummannaq vs. Ittoqqortoormiit (ab), Uummannaq vs. Tasiilaq (ac), Ittoqqortoormiit vs. Tasiilaq (bc). P-0.05*, P-0.01**, P-0.001***, nssnon-significant.

plasma levels of POPs in Greenlanders (Lagueux et al., 1999; Deutch and Hansen, 2000; Deutch et al., 2003) the comparisons were controlled for smoking, which made borderline associations highly significant. All the POPs were positively associated with the reported monthly intake of Inuit meals and, not surprisingly, several of them were inversely correlated with intake of Danish meals. Meals including seal meat were correlated with PCB, chlordanes, hexachlorobenzene and Mirex whereas meals with seal blubber alone were not correlated with concentrations of any POPs. However meals, which included seal products (meat, blubber, and liver) were significantly correlated with plasma levels of all POPs except DDE, but

in Tasiilaq only. Polar bear intake was significantly correlated with all POPs except DDE and Mirex, and so was intake of musk ox. However, the intake of musk ox is only common in Ittoqqortoormiit and may be a proxy variable for polar bear. Bird intake was correlated with PCB and Toxaphenes, and fish intake was correlated with all POPs except DDE and Toxaphenes, but in Tasiilaq only. All of these relationships were also tested for Uummannaq, but none of the associations between dietary factors and POPs were found to be significant, probably due to the lower number of participants (ns48). The associations between plasma phospholipid fatty acids (EPA, DPA, DHA and n-3yn-6) and

Table 4 Spearman bivariate correlations between monthly frequencies of meals (containing seal, polar bear, whale or fish. see Table 1), plasma fatty acids, and lipid adjusted POPs in three districts in Greenland, Uummannaq (U), Tasiilaq (T) and Itttoqqortoormiit (I) EPA, 20.5.3 Seal

U T I

0.33* 0.25* 0.26**

Polar bear

U T I

not asked– 0.002 ns 0.18 Ps0.08 ns

Whale

U T I

0.27 ns y0.03 ns 0.12 ns

Fish

U T I

0.24 Ps0.10 0.12 ns y0.07 ns

DPA, 22.5.3

DHA, 22.6.3

n-3yn-6

POPs噛

0.31* 0.26* 0.26*

0.33* 0.29* 0.24*

0.32* 0.27* 0.27**

ns positive** positive*

not asked– 0.18 ns 0.22*

not asked– 0.03 ns 0.25*

not asked– 0.07 ns 0.20*

not asked– positive* positive**

0.36* y0.01 ns 0.11 ns

ns ns ns

0.28 Ps0.05 0.15 ns y0.04 ns

ns positive** ns

0.32* 0.01 ns 0.14 ns 0.23 ns 0.16 ns y0.07 ns

0.28 Ps0.05 0.03 ns 0.18 ns 0.30* 0.19 ns y0.08 ns

Significance levels, P-0.05*, P-0.01**, nssnon-significant, 噛 correlations with five or more of the eight investigated POP types.

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Table 5 Associations between monthly meal frequencies and lipid adjusted POPs (controlled for smoking) in East Greenland (ns192) PCB aro1260

Beta HCH

Chlordanes

Danish meals, A Inuit meals, A Fish, A Game, A Seal, A Seal meat, F Seal blubber, F Seal, products, F (Tasiilaq only) Whale, A or F Whale blubber, F Polar bear, F Birds, F Fish, F Fish, F (Tasiilaq only) Musk ox, F

0.29**

0.26**

0.31**

DDE

Hexa chlorobenz.

y0.18*

y0.18*

0.28**

Mirex

PCB 14 congeners

Tox 5 congeners

y0.15 Ps0.05 0.30**

y0.17*

0.28**

0.27**

0.18*

0.15*

0.17* 0.19*

0.17*

0.26**

0.35**

0.23*

0.25** 0.16*

0.22**

0.24**

0.28**

0.24**

0.17* 0.38**

0.40**

0.38**

0.42**

0.24** 0.16*

0.23**

0.18*

0.20**

0.34**

0.27**

0.37**

0.25**

0.21*

0.28**

0.20**

0.19**

0.35**

0.33** 0.20**

Partial correlation coefficients and significance levels, P-0.05*, P-0.01**, P-0.001***. Only significant associations are shown. In Uummannaq, West Greenland (ns48) all associations were non-significant A. AMAP questionnaire, 10 local food categories, six possible monthly frequencies. F. Food frequency questionnaire, 35 local food categories, eight possible monthly frequencies.

plasma levels of all lipid adjusted POPs (microgram per kg total plasma lipid) were calculated for each town separately. All the associations were highly positive and significant Spearman r ranged from 0.30 to 0.75 (P-0.01**), which strongly indicates that the n-3 fatty acids and the lipophilic organic contaminants follow the same external sources and internal distribution. It also illustrates that a biochemical dietary indicator may be a more reliable marker of habitual dietary composition than a dietary questionnaire answer, although it is not quite as specific. Fig. 1a,b show the fatty acid ratio between DPA and EPA or DPA and DHA in ascending order in fat of marine animals which places them approximately at their respective trophic levels in the food chain. The fatty acid ratios are calculated from fatty acid data presented by Kuhnlein et al. (1991). The figure shows that the relative C22.5.3 content increases with higher trophic level and is very high in the marine top predators, namely polar bear, walrus, seal and toothed whales. The horizontal lines illustrate the mean human FA ratio-

levels in East Greenland (upper) and West Greenland (lower) and show that the inhabitants of East Greenland are higher level ‘predators’ than the inhabitants of West Greenland. Fig. 2a,b show the mean PCB levels in East Greenland (ns184) as a function of two fatty acids simultaneously, which indicates that PCB ( as well as other POPs, not shown) was more closely correlated with C22.5.3 than with the other n-3 Fatty acids. In fact there was almost no independent association with EPA and the correlation with DHA appeared to be negative. This finding strongly supports the suggestion that the most important external sources of POPs are those, which are rich in C22.5.3, namely polar bear, seal and walrus, which is in accordance with biomagnification of POPs through the marine food chain. The best models for predicting high blood levels of organic contaminants using PCB as an example (all other POPs analyzed in this study exhibited similar associations (Deutch and Hansen, 2000; Deutch et al., 2003) are shown in Table 6. These are, based either on questionnaire answers alone

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185

4. Discussion Within the last 5 years, most Arctic countries have performed one or more dietary surveys amongst their Indigenous populations, either as part of the Arctic Monitoring and Assessment Programme, (AMAP) Human Health programme, or as AMAP related or independent studies. These surveys have been performed for slightly different purposes using different target groups, sampling methods and reporting methods (Deutch, 2002). Some dietary surveys have determined and reported traditional food intake only, whereas others have included the total diet. Therefore comparisons

Fig. 1. Ascending ratios between n-3 fatty acids in marine animals vs. their approximate placement in food chain. Horizontal lines show the mean human levels of the same ratios.

or questionnaire answers in combination with biomarkers, C22.5.3 for diet and plasma cotinine for smoking. Both models are highly significant with high R-square values, 0.58 and 0.64, respectively. However, the model based upon the biomarkers performs significantly better than the other model. Using C22.5.3 as a predictor gave significantly better total R-square than using C20.5.3, C22.6.3 or n-3yn-6 ratio. If polar bear intake or seal intake were included singly, either one of them would be significant (Ps0.03* and 0.02*, respectively), but including both together yielded a better overall model.

Fig. 2. Mean human plasma PCB (microgramykg lipid) in East Greenland, ns184 as functions of two n-3 fatty acids in plasma phospholipids.

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Table 6 The two best models (multiple linear regression) predicting high plasma levels of PCB (logn lipid adjusted) in East Greenland (ns 192), questionnaire answers or biomarkers in plasma for diet and smoking. Standardized correlation coefficients and significance levels

Total adjusted R-square Age District (a) BMI Smoking (never, ever, now) Seal monthly meal intake Polar bear monthly meal intake Plasma cotinine ngyl Plasma C22.5.3,% of total phospholipids

Predicting plasma PCB (Questionnaire answers)

Predicting plasma PCB (Biomarkers in plasma)

0.58 0.52 P-0.0001*** y0.46 P-0.0001*** y0.152 Ps0.003** 0.146 Ps0.004** 0.100 Ps0.057 ns 0.083 Ps0.122 ns

0.64 0.367 P-0.0001*** y0.46 P-0.0001*** y0.136 Ps0.0004***

0.156 Ps0.002** 0.310 P-0.0001***

P-0.05*, P-0.01**, P-0.001***, nssnon-significant. (a) Ittoqqortoormiits1, Tasiilaqs2.

between countries and even between ethnic groups within countries can, in most cases, only are qualitative. The correlation between the intake of traditional food items, as measured by dietary surveys and blood levels of anthropogenic substances, has previously been demonstrated on both a group and population basis for heavy metals (Hansen, 1990) and for organochlorines (Van Oostdam et al., 1999). However, so as to more specifically analyze dietary risk behavior, this study has tried to demonstrate the correlation between individual dietary habits (relative and absolute intakes) and individual blood levels of xenobiotics. This problem is more complex due both to the large intra-personal variation in dietary behavior (day to day variation) and to the seasonal variation in traditional food availability. In addition, the persistent contaminants have been accumulated over a long time period (probably several decades) and dietary habits may have changed with time. However, long-term retrospective dietary surveys would have been less reliable than present day surveys. At present, the best indicators available for traditional food intake of marine origin are the relative concentrations of n-3 fatty acids in various human lipid fractions. The total plasma lipid fatty acid (FA) fractions indicate the most recent intakes and so are subject to day to day variations whereas the erythrocyte or plasma phospholipid FA frac-

tions determined in this study reflect the intake over a period of weeks. The FA fractions in adipose tissue, e.g. gluteal or subcutaneus fat reflect the more long term intake (Tjønneland et al., 1993; Deutch et al., 2000). Intervention studies with dietary supplements of n-3 fatty acids have shown significant changes of the n-3yn-6 ratio in plasma after 1–2 weeks and significant changes in gluteal fat over a period of 3–4 months (Deutch et al., 2000). The results of the combined analysis of questionnaire responses regarding consumption of local food, dietary markers such as fatty acids in plasma, and plasma levels of persistent organic pollutants, POPs, clearly confirm that traditional Inuit food, consisting of local marine mammals and fish, is the main source for the human burden of POPs. However, not all animals and fish are equally important contributors. This varies by district, local dietary preference and availability, and the local contaminant levels in subsistence animals. The local dietary habits show a common tendency in the three districts studied regarding the relative content of traditional food, which forms 25–30% of the total intake. However, there are differences in composition, which reflect both local geographic and climatic conditions and access to imported food. Ittoqqortoormiit, in North-East Greenland, is icebound for approximately 9–10 months of the year, which greatly reduces the

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availability of local fish and the variety of imported products. In contrast, although Tasiilaq is icebound for 7 months of the year, cod fishing is possible all year round. On the East coast, whale species are only available for a few months of the year, whilst in Uummannaq, icebound for approximately 6 months, fishing and whaling is possible year round. In both Ittoqqortoormiit and Uummannaq the diet relies heavily on large predatory marine mammals, whereas in Tasiilaq the diet is more westernised and more varied. The apparent overall consequence of this is that the human contaminant burden in Tasiilaq is significantly lower in than the other two districts. Animal contaminant data show that PCB and DDT levels are about twice as high in seals, birds, fishes and mussels caught in Ittoqqortoormiit than on the West coast (Johansen et al., 2000, 2002). This means that for the same intake of seals (or other marine animals) the exposure to contaminants is higher on the East coast than on the West coast. The multiple regression analysis of this study shows that the main predictors of high human burden of POPs are: age, BMI, district, consumption of seal and polarbear (or plasma phospolipid concentration of C22:5.3), and smoking (or plasma level of cotinine). Age is a predictor because the POPs are bioaccumulated over time, BMI is an (inverse) predictor probably due to a volume effect, which means that the lipophilic substances are distributed in a smaller volume in slim people, resulting in higher concentrations. As an illustration of this, Chevrier et al. (2000) found that the concentration of POPs in body fat increased in obese people who lost weight over a short time period. District is a predictor because of the uneven contaminant levels in local predatory animals (which have not yet been fully explained). Seal consumption is a predictor because it is the most ubiquitous food animal, and also has high POP levels. Polar bear is also an important food source particularly during the winter months, and the POPs levels in polar bear PCB especially are extremely high (AMAP, 1998)

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The finding that large predatory mammals are more important sources of POPs than most fish is supported by the linkage between POP levels and a specific fatty acid DPA, C22.5.3, which is more prevalent at higher trophic levels in aquatic animals. In human plasma acid fractions C22:5.3 only occurs as a low percentage of total lipid content (approx. 1%) and, therefore is seldom reported along with data for the other n-3 fatty acids. Our findings are also in accordance with other studies regarding POP exposure estimates from various subsistence animals (Johansen et al., 2000, 2002; Deutch, 2002, 2003). Although these exposure estimates should be regarded as provisional, they identify seal blubber (followed by whale blubber) as the predominant contributor to human PCB, DDT, chlordane, and HCH intake in West Greenland, whereas exposure via fish intake is infinitesimal. Regarding polar bear contamination, we do not, as yet, have sufficient data from the east coast of Greenland. However, contaminant data from other locations e.g. Svalbard (AMAP, 1998) indicates such high levels that polar bear would be the predominant source of PCB in areas where it is consumed (Deutch, 2003). This is in accordance with the correlation between reported polar bear intake and POP levels. Smoking is a predictor because consistently higher POPs levels among smokers indicate that nicotine or other substances in tobacco smoke influence the metabolism of these xenobiotic substances (Lagueux et al., 1999; Deutch and Hansen, 2000; Deutch et al., 2003). Due to polymorphism in genes coding for various enzymes involved in the metabolism and excretion of organochlorine compounds, e.g. CYP1A1 (Lagueux et al., 1999) the human tissue levels of POPs are also influenced by genetic factors. Furthermore, the tissue levels are influenced by various lifestyle factors such as body mass index, BMI (Deutch et al., 2003) and smoking (Lagueux et al., 1999; Deutch and Hansen, 2000; Deutch et al., 2003) where smoking is known to induce CYP1A1 activity (Lagueux et al., 1999). Therefore identification of individuals at risk of accumulating a high POP burden is not just a simple question of dietary exposure but is complicated by interacting genetic and biochemi-

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cal factors. These should receive more attention in future studies. This study investigated associations between self reported dietary habits, plasma fatty acids as dietary biomarkers, and plasma levels of a number of lipophilic persistent organic pollutants (11 pesticides and 14 PCB congeners) which are potentially toxic. Ultimately our intention is to enlarge on the basis for public health advice regarding dietary behaviour. This study has demonstrated the advantages of using biochemical markers of diet (fatty acids) and of smoking (cotinine) for more objective and reliable associations between contaminant levels and lifestyles and for validation of questionnaire answers. It has also shown that several of the n-3 fatty acids are good markers for marine food items and that each of the three long chain fatty acids, EPA, DPA and DHA may be used as specific markers. As shown in this study, DPA appears to be the most specific marker of high-level marine predators (mainly mammals) and thereby also of biomagnified lipophilic pollutants, whereas DHA is a better marker of fish intake. Finally, the study has shown that the relative dietary contribution to human organochlorine exposure varies according to local conditions and local dietary preference. Which means that public health measures and dietary counseling must take local conditions into consideration. References AMAP Assessment Report 1998. Arctic Pollution Issues. Bjerregaard P, Dewailly E, Ayotte P, Pars T, Ferron L, Mulvad G. Exposure of Inuit in Greenland to organochlorines through the marine diet. J Toxicol Environ Health part A 2001;62(2):69 –81. Chevrier J, Dewailly E, Ayotte P, et al. Body weight loss increases plasma and adipose tissue concentrations of potentially toxic pollutants in obese individuals. Int J Obesity Relat Metab Disord 2000;24(10):1272 –1278. Deutch B. Recent Dietary surveys in the Arctic. AMAP International Assessment report, 2002, Chapter 7. Deutch B. The Human Health Programme in Greenland 1997– 2001. In: Deutch B, Hansen JC, editors. The AMAP Danish

National Assessment report. The Danish EPA, Copenhagen, 2003. Deutch B, Hansen JC. High human plasma levels of organochlorine compounds in Greenland. Regional differences and lifestyle effects. Dan Med 2000;47(2):132 –137. Deutch B, Bonefeld Jørgensen E, Hansen JC. Ny3 PUFA from Fish or Seal oil reduce atherogenic risk indicators in Danish women. Nutr Res 2000;2(8):1065 –1077. Deutch B, Pedersen HS, Bonefeld-Jørgensen EC, Hansen JC. Smoking as a determinant of high plasma organochlorine levels in Greenland. Arch Environ Health 2003;58(1):1 –7. Dewailly E, Ayotte P, Bruneau S, Lebel G, Levallois P, Weber P. Exposure of the Inuit population of Nunavik (Arctic ` Quebec) to lead and mercury. Arch Environ Health 2001;56(4):350 –357. Hansen JC. Human exposure to metals through consumption of marine foods: a case study of exceptionally high intake among Greenlanders. In: Furness RS, Rainbow PS, editors. Heavy metals in the marine environment. Boca Raton, Florida: CRP Press, 1990. p. 227 –243. Hansen JC, Pedersen HS. Environmental exposure to heavy metals in North Greenland. Arctic Med Res 1986;41:21 – 34. Johansen P, Pars T, Bjerregaars P. Lead, cadmium, mercury and selenium intake by Greenlanders from local food. Sci Total Environ 2000;245:187 –194. Johansen P, Asmund G, Dietz R, Muir D. Contaminants in subsistence animals in Greenland. AMAP Danish National Assessment Report 2002, Chapter 3: pp. 19–50. Jul E, Mulvad G, Pedersen HS, Malcom GT, Hansen JC, Misfelt J. The relationship between a low rate of ischemic heart disease and the traditional Greenlandic diet with high amounts of monounsaturated and n-3 polyunsaturated fatty acids. Arctic Med Res 1994;suppl 2:282 –284. Kuhnlein H, Kubow S, Soueida R. Lipid components of traditional Inuit foods and diets of Baffin Island. J Food Compos Anal 1991;4:227 –236. Lagueux J, Pereg D, Ayotte P, Dewailly E, Poirier GG. Cytochrome P-450 CYP1A1 enzyme activity and DNA adducts in placenta of women environmentally exposed to organochlorines. Environ Res Section A 1999;80:369 –382. Pars T. Forbruget af Traditionelle grønlandske fødevarer. Ph.D. Thesis University of Copenhagen 2000. Tjønneland A, Overvad K, Thorling E, Ewertz M. Adipose tissue fatty acids as biomarkers of dietary exposure in Danish men and women. Am J Clin Nutr 1993;57:629 –633. Van Oostdam J, Gilman A, Dewailly E, Usher P, Wheatley B, Kuhnlein HV, et al. Human Health implications of environmental contaminants in Arctic Canada: a review. Sci Total Environ 1999;230:1 –82. Willet W. Nutritional Epidemiology. Oxford, UK: Oxford University Press, 1998. p. 174 –243.