Pollution indicators, fish consumption and the accumulation of mercury in human hair

Volume 15/Number 9/September 1984

stillbirth o r n e o n a t a l d e a t h in h u m a n s T h e m c k e l c o n c e n t r a t l o n in the l a n u g o o f s a i l - b o r n n n g e d seal p u p s is high c o m p a r e d to that f r o m the scalp h a i r o f m a n , w h i c h averages to a b o u t 1 p p m ( S t o e p p l e r , 1980) T h i s is a b o u t the s a m e level f o u n d in the hairs o f p u p s b o r n alive o r that o f the yearlings T h e s o u r c e o f m c k e l m L a k e S a i m a a is still u n c l e a r , a l t h o u g h t h e r e IS a c o n s i d e r a b l e a m o u n t o f i n d u s t r y in the a r e a ( H e l l e et a l , 1983) It m u s t b e r e m e m b e r e d t h a t the high m c k e l c o n c e n t r a t i o n in the h a i r o f s t i l l - b o r n p u p s m a y also b e a c o n s e q u e n c e o f s o m e m e t a b o h c d i s t u r b ance, w h i c h c o u l d b e the m a i n f a c t o r in t h e b a c k g r o u n d o f still-births

Fmancml support is gratefully acknowledged from Maj and Tor Nesshng FoundaUon and the World Wlldhfe Fund in Finland We would hke to thank Dr Eero Helle for his valuable help in preparing the paper

Frost, K J & Lowry, L F (1981) Ringed, Bmkal and Caspmn seals In Handbook of Marine Mammals (S H Radgway & R J Harrison, eds ) pp 29-53 Academac Press, New York

Helle, E, Hyvarmen, H & Slpda, T (1981) The last chance to save the Smmaa nnged seal (In Fmmsh with Enghsh summary) Suomen Luonto, 8, 423-425 Helle, E, Hyvarmen, H, Pyysalo, H & Wtckstrom, K (1983) Levels of organochlonne compounds m an roland seal population m eastern Finland Mar Pollut Bull, 14, 260-263 Hyvarmen, H & Slpda, T (1983) The Salmaa seal (m Fmmsh wffh Enghsh summary) Tlede 2000 Hasanen, E (1975) Elohopea ympanstoongelmana Suomessa Ympanstola Terveys,7,515-528 Jones, D, Ronald, K, Lavlgne, D M, Frank, R, Holdrmget, M & Uthe, J F (1976) Organochlorlne and mercury residues m the harp seal (Pagophdusgroenlandtcus) Sct Total Envtr, 5, 181-195 Karl, T & Kauranen, P (1978) Mercury and selenmm contents of seals from fresh and brackish water m Finland Bull envtr Contam Toxtc, 18,273-280 Karppanen, E & Henrlkson, K (1974) Kvlcksdver och kiorerade kolvatehalter 1 havs och -msjosalar Suomen Elamlaakardehu, 80, 378-391 Martin, J H, Elhot, P D, Anderhnl, V C, Glrvln, D, Jacobs, S A, Rlseborough, R W, Delong, L R & Gdmartm, W G (1976) Mercury-selemum-brom~de imbalance m premature parturient California sea hons Mar Btol, 35, 91-104 Schroeder, H A & Mltchener, M (1971) Toxic effects of mace and rats Archs envtr Hlth , 18,473-479 Smath, T & Armstrong, F A J (1978) Mercury and selenium m rmged and bearded seal tissues from arcuc Canada Arcttc, 31, 75-84 Stack, M V, Burkltt, A J & Nlckless, G (1976) Trace elements in teeth at birth (1957-1963 and 1972-1973) Bull envtr Contam Toxtc, 16, 746-766

(1025-326X/84 $3 00+0 00 © PergamonPressLtd

Martin Pollunon Bulletin Vol 15 No 9 pp 337-340 1984 Printed m GreatBritain

Pollution Indicators, Fish Consumption and the Accumulation of Mercury in Human Hair D AIREY Division o f Oceanography, C S I R O Marine Laboratories, P O B o x 21, Cronulla, N S W 2230, Austraha

Mercury can accumulate in the human body from fish and from other environmental sources, and the amount accumulated is indicated by hair mercury concentration. Anthropogenic mercury losses in many countries have been correlated with Gross National Product (GNP, an indicator of industrial activity), and industrial density (represented by GNP/land area, i.e. GNP/LA) has been used as an indicator of potential pollution for coastal fishing grounds. For a data set taken from the literature, 30% of the 54% variability in hair mercury concentrations explained by national fish consumption can also be explained by GNP/LA. However, using new data, the effect of GNP and GNP/LA on the amount of mercury accumulated in hair of people from many countries was insignificant compared to the effect of national fish consumption. 74.1% of the variability in the hair mercury levels of people who ate the same number of meals offish was explained by the national average fish consumption. This suggests that fish species and fish size are more important than general indicators of mercury pollution when estimating the mercury accumulation in humans on an international scale.

C o m p a r e d with d e v e l o p i n g nations, c o u n t r i e s with high G N P g e n e r a l l y u s e m o r e m e r c u r y in m d u s t n a l p r o c e s s e s , discharge more mercury waste and release more m e r c u r y w h e n b u r m n g fossd fuels for e n e r g y o r p r o c e s s xng o r e s at high t e m p e r a t u r e ( A l r e y , 1 9 8 2 , G o l d b e r g , 1976) M o s t c o u n t r i e s with the highest G N P s a r e s~tuated in the n o r t h e r n h e n u s p h e r e ( G o l d b e r g , 1 9 7 6 ) w h e r e air ( S l e m r et a l , 1981), s e a w a t e r ( G a r d n e r , 1 9 7 5 ) a n d h a i r (Alrey, 1982) have higher mercury concentrations than in t h e s o u t h e r n h e m i s p h e r e W h e r e s e a w a t e r m e r c u r y c o n c e n t r a t i o n s a r e l'ugh, so a r e the m e r c u r y c o n c e n t r a tions o f t h e fish h v m g m t h o s e w a t e r s ( G a r d n e r , 1 9 7 8 ) G o l d b e r g ( 1 9 7 6 ) has h y p o t h e s i z e d that a high G N P / L A c a n b e an a p p r o x i m a t e m d i c a t o r o f c o u n t r i e s with p o l l u t e d c o a s t a l w a t e r s M o s t c o a s t a l o r island c o u n t r i e s with small l a n d a r e a s h a v e a l m u t e d a m o u n t o f c o a s t l i n e f o r r e c r e a t i o n , waste discharges, h a r b o u r facilities, c o o l m g w a t e r a n d s e a f o o d industries so if such c o u n t r i e s also h a v e a high G N P , the p r o b l e m is e x a c e r b a t e d It is k n o w n that m e r c u r y a c c u m u l a t e s in the h u m a n b o d y f r o m fish and from other environmental sources (Fnberg & 337

M a n n e Pollution Bulletin Personal and international variables

Mercury accumulation I In merlne food chain

I

L_ ~ N u [~Mercury in fish Anthropogonic ~ , Natural

m b e r of fish meals a month, A, B, C L..._ - Amount of fish In a meal ~,---'~Specles of fish consumed ~--'LSize of fish consumed

~ N a t l o n a l

average fish consumption

Mercury accumulation [ in air, food & water natural + anthropogonic [ (GNP or GNP/LA?) [

Mercury accumulation In man represented by hair mercury concentrations

Ftg

[

1 Environmental mercury pathways mto h u m a n hmr

Nordberg, 1972, Alrey, 1983c) Therefore how much effect does industrial activity have on the accumulation of mercury in humans 9 Is mercury pollution a hazard only to those people hvmg close to or eating fish from waters near industrial areas, e.g Mmamata Bay 9 The amount of mercury accumulated m the human body is indicated by hair mercury concentrations (Phelps et al, 1980) I have shown elsewhere (Alrey, 1983a) that throughout the world, hair mercury levels are highest in people who consume fish most frequently but each country has different mean levels for people who ate fish once a month (A), tw-tce a month (B) and four times a month (C) The present work tests whether the international &fferences in mean hair mercury concentratlons can be explained by general pollution indicators (GNP and GNP/LA) or by national average fish consumption or by other factors such as fish specws or fish size (see F]g 1)

Methods Two data sets (Alrey, 1983a,b) were used to investigate these questions. Data set I was compded from the hterature and includes anthmetac mean halr mercury concentratmns from more than 9000 people from 185 locations m 35 countries Data set II was composed of hair samples from 538 people who hved in 30 locatmns

in 13 countnes, analysed by a standard method (Gardner & Dal Pont, 1979, Gardner, 1980) m a clean-room (Gardner, 1979) The reproduclblhty of the method was tested and 15 replicates of roughly chopped hair sample had 2 445:0 13 ppm mercury (Alrey, 1983a). For both data sets hair mercury concentrations in people occupaUonally exposed to mercury, m people who ate fish every day or ate fish known to be heavily contarmnated with mercury, and hair mercury concentrations winch were orders of magmtude tugher than normal were excluded The difference between data sets I and II are (1) II excludes vanablhty due to rater-laboratory analytical errors (n) Hair samples in II were collected In 1979-1980 whtle data m I was reported from 1965-1981 and would include any long-term vanablhty in hair mercury levels

Results Table 1 shows the regressions of mean hair mercury concentrations on national fish consumption and GNP (GNP/LA was lnslgraficant for all regressions) For equations 1-4, the mean hair mercury concentrations from all locations in each country were used and the per captta fish consumption was Ignored The dtfference (29 3% compared to 69 4%) in the variance in hair mercury concentrations accounted for by national fish

TABLE 1 Regression of mercury hatr concentrauons on national fish c o n s u m p t m n and Gross National Product

Data set

Standard errors fish

GNP

(1) Hg -- 1 67 + 0 13 FISH (2) H g - - 1 5 1 + 0 10 FISH + 0 44 G N P

0 01 001

(3) Hg - 1 11 + 0 08 FISH (4) Hg - 0 94 + 0 08 FISH + 0 47 G N P

0 01 0 01

Equation

I (locaUon)

II (locaUons)

II (countries) A A I)

I)

(5) (6) (7) (8) (9) (10)

Hg R Hg-Hg-HgHg Hg--

0 78 + 0 07 FISH 0 63 + 0 07 FISH + 0 4 1 G N P 1 08+008FISH 1 2 5 + 0 13 FISH 1 05 + 0 095 FISH 0 95 + 0 093 FISH + 0 30 G N P

0 02 002 002 002 0 02 002

Hg - mean hmr mercury concentration m each country (ppm) FISH - Average annual fish c o n s u m p u o n (kg/person) (F O A , 1978) G N P - Annual Gross National Product (SUS × 1012) (World Bank, 1979) * -- 100 ([total mean square (MS)--Restdual MS]/total MS) - P DF - degrees of freedom I, II data sets--see text A, B C, Data for donors who ate fish once or less, twice, four Umes a m o n t h NS -- Not s~gmficant

15 A+B+t2 3

338

DF

SIgmflcance Fish GNP

Percentage variance* accounted for

033

184 184

0 005 0005

010

29 0 293

0 22

29 29

0 005 0 005

0 05

65 4 69 4

11 11 10 10 10 10

0 005 0005 0005 0005 0 005 0005

027

029

NS

NS

58 6 631 612 824 74 1 746

Volume 15/Number 9/September 1984

70

6G 5G >,40 o

E30 -r 2O 10 00(~

I

I

I

1

4 8 112 ll6 20 214 28 312 316 gO National filh consumption (kg/head/year)

Fig 2 Mean hmr mercury concentrations of donors who ate fish weekly against nat]onal average fish consumption

consumption and G N P between data sets I and II is probably due to differences in analytical and samphng methodology Using data set II the mean hair mercury concentrations for each country were calculated for donors m three groups those who ate one or less (A), two (I]) and four ((2) fish meals per month The mean for each country (I)) was calculated as the mean of these three values For these regress]ons G N P had no significant effect on the variance accounted for The national average fish consumption explmns a high percentage of the varmblhty for all groups F o r group (2 tins was 82 4% and for the combined data I3 it was 74 1% Figure 2 is an example of the correlation between mean hmr concentrations (group (2) and national average fish consumption The correlations were tested without Japan winch could have forced the result, however, the correlations were still slgmficant it should be remembered that we hve in a world of finite size and additional data between that for Japan and Hong Kong (the higher values m Fig 2) may not exist

national fish consumption could also be explained by mercury pollution as indicated by G N P or G N P / L A Parual correlation coefficients are used to determine what part of a correlataon between two vanables (hmr mercury concentraUons and national fish consumption) is not a reflecUon of their relation wtth a tinrd vanable (GNP or G N P / L A ) If the third variable is held constant at any value and the correlation between the first two variables ]s approximately the same as the simple correlation between them, then the relatlonsinp between the first two variables Is independent of the tinrd variable Conversely, if the partial correlation coefficient is different to the simple correlaUon coeffioent, then the first two vanables are dependent on the tinrd vanable The formula (Snedecor & Cochran, 1967) for the partxal correlation coeffioent between variable 1 and 2 holding 3 constant is r~23 ----lr~2 - r13 r23] [(1 -- ~3) (1 - r223)]-1/2 where simple correlation coefficwnts between variable 1, 2, 3 are given by r~2, r~3 and r23 Smallar formulae can be written for rt32 and r23 Now ff the vanables are hair mercury concentration (H), national fish consumption (F), GNP ( G ) and G N P / L A (L), the simple correlation coefficients for data set I (185 locations) are

r.F---- 0 54 ++ rilL = 0 50 ++ rnG ==0 25 ++ reG----0 33 ++ and partial correlation coeffioents are

rnFo=050 ++ rHFL=024 ++

rt4Lf~011

rnor010

For data set II (30 locations) the simple correlation coefficients are rn~--0 81 ++

rUL=058 ++

rHO----041 +

rF6~ 0 22

and partaal correlation coeffioents are

r14F~O 81 ++ rItFL~-O71 ++ rt4Leffi--O 24 rnGt~O 42 + and for data set II (13 countnes) the sunple correlaUon coeffioents are

rnr=O 88 ++

rnc=O 37

rn6~O 25

and partml correlation coefficients are

Discussion In calculating the regression for the mean hmr mercury levels m each country It was assumed that each fish meal contained the same amount of fish of average mercury content, and the donors' stated fish consumption was the same lnternat~onally So the result that 74 1% of the variance m the mean hmr mercury concentrations could be accounted for by national average fish consumption, was unexpected The amount of fish eaten per capita by the donors represented by equations 1 - 4 was variable so national fish consumption might be expected to influence how much was eaten and hence the hair mercury concentrations However, m equations 5 10, where each group ate the same quant]ty of fish, I expected that national fish consumption would have httle ff any effect and that any international vanabdlty might be explained by G N P or G N P / L A Therefore I compared simple and partial correlation coefficients to estimate whether the correlation accounted for by the

rnec-~-O 89 ++ rnFL=O 86 ++ rncFffiO 36 rnLeffi--O 09 When the significant correlations only are used, the following results are obtained (slgmficant at 5% level +, and 1% level ++) For data set I the correlation coeffic]ents rnFaffi 0 50, rneL=O 24 compared with rnr=O 54 shows that of the 54% correlation between hair mercury levels and national fish consumption, only 4% can be accounted for by G N P winle 30% can be explained by G N P / L A For data set II (locations) r14Fa~ 0 81 and r14FC=0 71 compared to r m ~ 0 81 shows that none of the correlation between hmr mercury levels and national fish consumption ~s explained by changing G N P and only 10% by changing G N P / L A For data set II (countnes) rHFG~ 0 89 and rHFL~ 0 86 compared to rn#= 0 88 shows that almost none of the correlauon between hair mercury levels and national fish consumption Is explained by changing G N P or G N P / L A 339

Marine Pollution Bulletm F o r d a t a set I o n l y 2 9 % o f t h e v a r i a t i o n ( r 2) in the m e a n hair m e r c u r y levels is e x p l a i n e d b y n a t i o n a l a v e r a g e fish c o n s u m p t i o n , while for d a t a set I 1 6 5 % o f t h e t o t a l v a n a tlon is e x p l a i n e d b y n a t i o n a l fish c o n s u m p t i o n T h e p a r t i a l c o r r e l a t i o n coefficients f o r d a t a set I s h o w that GNP/LA explains a substantial amount of the correlation b e t w e n h a i r m e r c u r y levels a n d n a t i o n a l fish c o n s u m p t i o n w h i c h suggests that b e t w e e n 1965 a n d 1981 p e o p l e ate c o n t a m i n a t e d fish f r o m c o a s t a l w a t e r s b u t f o r d a t a set II G N P o r G N P / L A h a v e o n l y a v e r y small c o n t n b u l a o n to t h e c o r r e l a t i o n suggesting that p e o p l e in 1 9 7 9 - 8 0 ate v e r y httle c o n t a r n m a t e d fish f r o m c o a s t a l w a t e r s B e c a u s e o f difference in the b a s e s o f d a t a set I a n d II m e n t i o n e d a b o v e , t h e s e suggestions a r e s p e c ulative a n d c a n n o t b e r e s o l v e d unUl d a t a set I is r e p l a c e d b y o n e large e n o u g h for statistical analysis, b u t w h i c h is n o t s p o d e d b y v a n a b t l l t y d u e to analytical t e c h n i q u e s W h e n the fish c o n s u m p t i o n o f the d o n o r s was fixed, 1e groups A-D, neither GNP nor GNP/LA contributed to the c o r r e l a t i o n A l s o the c o r r e l a t i o n coefficients b e c a m e c l o s e r to o n e as the n u m b e r o f fish m e a l s p e r m o n t h i n c r e a s e d , l e r H G ---- 0 79, 0 81 a n d 0 92 f o r g r o u p A , 1) a n d C r e s p e c t i v e l y This suggests that the elev a t e d h a i r m e r c u r y levels a s s o c i a t e d w~th m o r e f r e q u e n t c o n s u m p t i o n o f fish a r e affected less b y o t h e r v a r i a b l e s such as m e r c u r y Intake f r o m air, d e n t a l fillings a n d f o o d stuffs o t h e r t h a n fish, a n d sex a n d age o f t h e d o n o r s So w h y d o e s n a t i o n a l fish c o n s u m p t i o n c o r r e l a t e with hair m e r c u r y levels f o r p e o p l e eating the s a m e n u m b e r o f fish meals9 T h e p o s s i b i h t l e s a r e s h o w n m F i g 1 N o s u r v e y has y e t b e e n m a d e to c o m p a r e the a m o u n t o f fish in a m e a l m different c o u n t n e s H o w e v e r , o n e can s p e c u l a t e that the p e o p l e m c o u n t r i e s w h i c h h a v e high n a t i o n a l a v e r a g e fish c o n s u m p t i o n s t e n d to eat a large n u m b e r o f fish which n a t u r a l l y c o n t a i n high levels o f mercury, e g J a p a n e s e eat b l a c k m a r h n , tuna, s h a r k a n d whales (FAO, 1978) H o w e v e r , it lS i m p o s s i b l e at p r e s e n t to calculate the a m o u n t o f m e r c u r y e n t e r i n g the fish s h o p s in e a c h c o u n t r y in i n d w l d u a l species, b e c a u s e o f t h e lack o f d a t a o n the size o f fish c a u g h t o r i m p o r t e d a n d the m e r c u r y c o n c e n t r a t i o n s In different sizes So t h e q u e s t i o n r e m a i n s to b e a n s w e r e d a n d the d a t a p r e s e n t e d

340

h e r e c a n o n l y suggest that, in r e c e n t ttmes, o n a g l o b a l scale m e r c u r y p o l l u t i o n r e p r e s e n t e d e i t h e r as G N P o r G N P / L A d i d n o t influence the a c c u m u l a t i o n o f m e r c u r y in h u m a n s F o r small p o p u l a t i o n s e a t m g fish f r o m locally c o n t a n u n a t e d w a t e r s this is n o t valid A l s o I b e l i e v e the size a n d s p e c i e s o f fish e a t e n o r v a r i a b i l i t y m the size o f a m e a l c o n t a t m n g fish m u s t have s o m e effect I thank D Retd, CSIRO Dwlsion of Mathematics and StaUstlcs, and D Crooks, CSIRO Manne Laboratories, for help with computations G Dalpont for techmcal assistance and colleagues and friends who collected hmr samples Atrey, D (1982) Contributions from coal and mdustnal matenals to mercury m mr, rainwater and snow Set total Enwr, 25, 19-40 Atrey, D (1983a)- Total mercury concentration m human hmr from 13 countries m relation to fish consumption and location Set totalEnvtr, 31,681-686 Alrey, D (1983b) Acompdatlonofhmrmercurylevelsfrompopulatlons throughout the world also showing gross national product, coal, mercury, thermal energy and fish consumption of each country Aust CSIRO Mar Lab Mwrofiche Rep 4

Aarey, D (1983c) Mercury m human hair due to environment and dlet--a review Envlr Hlth Perspect , 52,303-320 F A D (1978) Year Book ofFtshenes Stanstws, Vol 44 Umted Nations, Rome Fnberg, L & Nordberg, G F (1972) Inorgamc mercury, relation between exposure and effects In Mercury tn the Envtronment (L Fnberg & J Vostal, eds ), pp 113-139 C R C Press, Cleveland, OH Gardner, D (1975) Observations on the distribution of dissolved mercury m the ocean Mar Pollut Bull, 6, 43-46 Gardner, D (1978) Mercury m waters and fish of the Irish Sea and other UK fishing grounds Nature, Lond, 272, 49-51 Gardner, D (1979) A laminar flow clean room for trace metal analysis in manne chemistry Lab Pmct, 28, 1071-1075 Gardner, D (1980) The use of magnesmm perchlorate as desiccant in the syringe mlecuon techmque for deterrnmatlon of mercury by cold vapour atomic absorption spectrophotometry Anal Chtm Acta, 119,167-169 Gardner, D & Dal Pont, G (1979) A rapid simple method for determxnaUon of total mercury m fish and hmr Anal Chtm Acta, 108, 13-20 Goldherg (ed) (1976) Health of the Ocean~ UNESCO Press, Pans Phelps, R W, Clarkson, T W Kershaw T G & Wheatley, B (1980) Inter-relationships of blood and hmr mercury concentrations m a North Amencan population exposed to methyl mercury Archs Envtr Hlth, 35, 161-168 Slemr, F, Seder, W & Schuster, G (1981) Latltudmal distribution of mercury over the Atlantic Ocean J geophys Res, 86, 1159-1166 Snedecor, G W & Cochran, W G (1967) Stattstwal Methods, 6th ed State Umv Press, Ames, Iowa World Bank (1979) Atlas of Population Per Captta Product and Growth Rates, pp 1-23 World Bank, Washington