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Bioaccumulation in marine food chains—A kinetic approach
Marine Environmental Research 17 (1985) 29%300
Bioaccumulation in Marine Food Chains-A Kinetic Approach
C. H. W a l k e r Department of Physiology and Biochemistry, University of Reading. PO Box 228, Whiteknights, Reading RG6 2AJ, Great Britain
The risk of bioaccumulation of persistent liposoluble pollutants in marine food chains was highlighted by work done on organochlorine residues in marine organisms in the early 1960s. In one study, concentrations of DDE and dieldrin were determined in species from different trophic levels of the Farne Island ecosystem. L Concentrations of pollutants were related to trophic levels, with the highest levels occurring in predators such as the cormorant (Phalacrocorax carbo) and the shag (Phalacrocorax aristotelis). This paper will consider model systems which may be used to predict bioaccumulation risks from simple in vitro data. Emphasis will be upon persistent liposoluble pollutants with relatively simple patterns of metabolism, and upon the problem of bioaccumulation by marine predators. B I O A C C U M U L A T I O N A N D B I O C O N C E N T R A T I O N BY A Q U A T I C SPECIES In the simplest situation the uptake and loss of a compound by an aquatic organism can be described by a one compartment model. Where metabolism is unimportant and uptake and loss are very largely by simple passive diffusion then the bioconcentration factor for a compound C]C o is related to its partition coefficient 2 between water and a nonpolar liquid, where C~ = concentration within organism C o = concentration in ambient water 297 Marine Environ. Res. 0141-1 [ 36/85/$03.30 C Elsevier Applied Science Publishers Ltd, England, 1985. Printed in Great Britain
298
C. H. Walker
A similar relationship exists for the water solubility of a compound because this is related to the partition coefficient. Ernst 2 obtained a good inverse correlation between the logs of the water solubilities of seven lipophilic organochlorine compounds and the logs of their bioconcentration factors in M v t i l u s edulis under steady state conditions. Similarly. Neely et al. showed a good correlation between the logs of the octanol:water partition coefficients of either organic compounds and the iogs of their bioconcentration factors in rainbow trout (Salmo gairdnerii). 3
However, in many situations bioconcentration or bioaccumulation is not well predicted by partition coefficients or water solubilities. Norstrom et al. ~ developed a more complex model for the long term bioaccumulation of pollutants by fish which takes into account uptake f[om both food and water, and also the diluting effect of growth. The following general equation was given dC, [rate of uptake rate of uptake] [rate clearance rate o f ] d,' = L from water + from food ] - [ from tissue + growth] where C, = concentration in fish and t = time.
B I O A C C U M U L A T I O N BY M A R I N E P R E D A T O R S With marine predators such as fish-eating birds, equations for bioaccumulation of persistent liposoluble compounds can be developed if the following assumptions are made: (i) that nearly all uptake of a compound is via the food: (ii) that there is little excretion of unchanged compound; (iii) that most of the metabolism occurs in the liver. Under steady state conditions rate of uptake = rate of loss of compound (units, mg/kg;day) of compound This can be written as concentration in food (Co) (mg/kg) x A t. 0.5 x C i ( m g k g ) days required for animal to consume - initial tso (days) own weight in food (N) (At-= fraction of C O which is absorbed)
Bioac'cumulation in n,arine jbod chains
299
which can be rearranged to give bioaccumulation factor (BF) = C-AL= 2At x initial tso CO N Application of this equation to data from a pharmacokinetic study on dieldrin in the male rat gave a predicted BF of 0' 11, which compared well with an actual BF of 0.1-0.15 (see Ref. 5). Several studies have shown that rates of metabolism of liposoluble c o m p o u n d s measured in vitro reasonably predict rates of metabolism or excretion in rico (see Ref. 6). Thus it is worth considering the use of in vitro kinetic data, which are relatively easy to obtain, to predict bioaccumulation /'actors. Where steady state kinetics apply the rate of absorption of a c o m p o u n d is equal to its rate of loss. In the present case the rate of loss approximates to the rate of metabolism by the liver. This can be described by an adaptation of a two compartment model where the liver represents a central compartment in equilibrium with the other tissues of the body at the steady state (Fig. 1). The rate of uptake of lipophilic c o m p o u n d s from the gut and from the tissues is balanced by the rate of loss by metabolism and by redistribution to the tissues. This can be written 1 C o × A t. x ~ =
app Vma x X C L app K m + C L
where app Vm~~ is given in units of mg substrate/kg body wt/day and app
•
~
I
Peripheraltissues distribution
Out-~ Liver
~ x ~
bolism(Excretion) Fig. I. Liver kinetics--an adaptation of a two compartment model where the liver represents a central compartment, in equilibrium with the other tissues of the body at the steady state (C L=concentration in the liver).
300
C. H. Walker
K m is expressed as ppm in terms of liver or liver microsomes. Both of these constants can be determined in citro with liver preparations. C L is the concentration in the liver. If Lineweaver-Burke plots are constructed, the relationship is shown between 1 c and 1 Ct. where v is the velocity of reaction expressed in the same units as/"m~.v Since velocity is equal to the rate of uptake, values for Ct. can be deduced from this graph for any rate of uptake. If Cb/Q is known at the steady state, C~ and BF C~/Co can now be determined. Where rate of metabolism is rapid in relation to rate of redistribution from the liver, then the rates of metabolism and excretion should not be limited by enzyme activity, i.e. changes in enzyme activity should not significantly affect the rate of metabolism because the metabolic capacity is sufficiently high to break down most of the c o m p o u n d entering the liver. By contrast, where the two processes proceed at similar rates, the enzyme activity could be rate-limiting.
REFERENCES 1. Robinson, J., Richardson, A.. Crabtree, A. N., Coulson, J. C. & Potts, G. R. Nature, 214, 1307-11 (t967). 2. Ernst, W. Chemosphere, 11,731-40 (1977). 3. Neely, W. B., Branson, D. R. & Blau, G. E. J. Eric. Sci. Tech., 8, 1113-15 (1974). 4. Norstrom, R. J., McKinnon, A. E. & de Freitas, A. S. W. J. Fish. Res. Board Can., 248-67 (1976). 5. Moriarty, F. In Organochlorine Insecticides in Persistent Organic" Pollutants, Academic Press, London, pp. 29-40, 1975. 6. Walker, C. H. Progr. Pestle. Biochem., 247-85 (1981).
Bioaccumulation in Marine Food Chains-A Kinetic Approach
C. H. W a l k e r Department of Physiology and Biochemistry, University of Reading. PO Box 228, Whiteknights, Reading RG6 2AJ, Great Britain
The risk of bioaccumulation of persistent liposoluble pollutants in marine food chains was highlighted by work done on organochlorine residues in marine organisms in the early 1960s. In one study, concentrations of DDE and dieldrin were determined in species from different trophic levels of the Farne Island ecosystem. L Concentrations of pollutants were related to trophic levels, with the highest levels occurring in predators such as the cormorant (Phalacrocorax carbo) and the shag (Phalacrocorax aristotelis). This paper will consider model systems which may be used to predict bioaccumulation risks from simple in vitro data. Emphasis will be upon persistent liposoluble pollutants with relatively simple patterns of metabolism, and upon the problem of bioaccumulation by marine predators. B I O A C C U M U L A T I O N A N D B I O C O N C E N T R A T I O N BY A Q U A T I C SPECIES In the simplest situation the uptake and loss of a compound by an aquatic organism can be described by a one compartment model. Where metabolism is unimportant and uptake and loss are very largely by simple passive diffusion then the bioconcentration factor for a compound C]C o is related to its partition coefficient 2 between water and a nonpolar liquid, where C~ = concentration within organism C o = concentration in ambient water 297 Marine Environ. Res. 0141-1 [ 36/85/$03.30 C Elsevier Applied Science Publishers Ltd, England, 1985. Printed in Great Britain
298
C. H. Walker
A similar relationship exists for the water solubility of a compound because this is related to the partition coefficient. Ernst 2 obtained a good inverse correlation between the logs of the water solubilities of seven lipophilic organochlorine compounds and the logs of their bioconcentration factors in M v t i l u s edulis under steady state conditions. Similarly. Neely et al. showed a good correlation between the logs of the octanol:water partition coefficients of either organic compounds and the iogs of their bioconcentration factors in rainbow trout (Salmo gairdnerii). 3
However, in many situations bioconcentration or bioaccumulation is not well predicted by partition coefficients or water solubilities. Norstrom et al. ~ developed a more complex model for the long term bioaccumulation of pollutants by fish which takes into account uptake f[om both food and water, and also the diluting effect of growth. The following general equation was given dC, [rate of uptake rate of uptake] [rate clearance rate o f ] d,' = L from water + from food ] - [ from tissue + growth] where C, = concentration in fish and t = time.
B I O A C C U M U L A T I O N BY M A R I N E P R E D A T O R S With marine predators such as fish-eating birds, equations for bioaccumulation of persistent liposoluble compounds can be developed if the following assumptions are made: (i) that nearly all uptake of a compound is via the food: (ii) that there is little excretion of unchanged compound; (iii) that most of the metabolism occurs in the liver. Under steady state conditions rate of uptake = rate of loss of compound (units, mg/kg;day) of compound This can be written as concentration in food (Co) (mg/kg) x A t. 0.5 x C i ( m g k g ) days required for animal to consume - initial tso (days) own weight in food (N) (At-= fraction of C O which is absorbed)
Bioac'cumulation in n,arine jbod chains
299
which can be rearranged to give bioaccumulation factor (BF) = C-AL= 2At x initial tso CO N Application of this equation to data from a pharmacokinetic study on dieldrin in the male rat gave a predicted BF of 0' 11, which compared well with an actual BF of 0.1-0.15 (see Ref. 5). Several studies have shown that rates of metabolism of liposoluble c o m p o u n d s measured in vitro reasonably predict rates of metabolism or excretion in rico (see Ref. 6). Thus it is worth considering the use of in vitro kinetic data, which are relatively easy to obtain, to predict bioaccumulation /'actors. Where steady state kinetics apply the rate of absorption of a c o m p o u n d is equal to its rate of loss. In the present case the rate of loss approximates to the rate of metabolism by the liver. This can be described by an adaptation of a two compartment model where the liver represents a central compartment in equilibrium with the other tissues of the body at the steady state (Fig. 1). The rate of uptake of lipophilic c o m p o u n d s from the gut and from the tissues is balanced by the rate of loss by metabolism and by redistribution to the tissues. This can be written 1 C o × A t. x ~ =
app Vma x X C L app K m + C L
where app Vm~~ is given in units of mg substrate/kg body wt/day and app
•
~
I
Peripheraltissues distribution
Out-~ Liver
~ x ~
bolism(Excretion) Fig. I. Liver kinetics--an adaptation of a two compartment model where the liver represents a central compartment, in equilibrium with the other tissues of the body at the steady state (C L=concentration in the liver).
300
C. H. Walker
K m is expressed as ppm in terms of liver or liver microsomes. Both of these constants can be determined in citro with liver preparations. C L is the concentration in the liver. If Lineweaver-Burke plots are constructed, the relationship is shown between 1 c and 1 Ct. where v is the velocity of reaction expressed in the same units as/"m~.v Since velocity is equal to the rate of uptake, values for Ct. can be deduced from this graph for any rate of uptake. If Cb/Q is known at the steady state, C~ and BF C~/Co can now be determined. Where rate of metabolism is rapid in relation to rate of redistribution from the liver, then the rates of metabolism and excretion should not be limited by enzyme activity, i.e. changes in enzyme activity should not significantly affect the rate of metabolism because the metabolic capacity is sufficiently high to break down most of the c o m p o u n d entering the liver. By contrast, where the two processes proceed at similar rates, the enzyme activity could be rate-limiting.
REFERENCES 1. Robinson, J., Richardson, A.. Crabtree, A. N., Coulson, J. C. & Potts, G. R. Nature, 214, 1307-11 (t967). 2. Ernst, W. Chemosphere, 11,731-40 (1977). 3. Neely, W. B., Branson, D. R. & Blau, G. E. J. Eric. Sci. Tech., 8, 1113-15 (1974). 4. Norstrom, R. J., McKinnon, A. E. & de Freitas, A. S. W. J. Fish. Res. Board Can., 248-67 (1976). 5. Moriarty, F. In Organochlorine Insecticides in Persistent Organic" Pollutants, Academic Press, London, pp. 29-40, 1975. 6. Walker, C. H. Progr. Pestle. Biochem., 247-85 (1981).