Chemosphere, Vol.20, Nos.7-9, pp 779-786, 1990 0045-6535/90 $3.00 + .OO Printed in Great Britain Pergamon Press plc

THE USE OF BIOCONCENTRATION FACTORS IN ESTIMATING THE 2,3,7,8-TCDD CONTENT OF COW'S MILK

Thomas Webster* and Paul Connett

*Center for the Biology of Natural Systems, Queens College, Flushing, NY 11367

Chemistry Department, St. Lawrence University, Canton, NY 13617

ABSTRACT

Five models for estimating the 2,3,7,8-TCDD contamination of cow's milk from air are compared with field data from a known source of dioxin in Austria. Bioconcentration from soil is a very minor pathway for contamination of hay in this setting, leading to underpredictions of greater than an order of magnitude. Direct deposition of particulate produces better results, but vapor transfer of PCDD/PCDF to plants should be considered. A bioconcentration factor from dry hay to milk fat of 1.7 was observed, less than that assumed by the five models. 2,3,7,8-TCDD equivalents transferred from air to milk fat less efficiently than 2,3,7,8-TCDD. Important model parameters should be based on experiments which accurately represent the modelled situation.

KEYWORDS

Bioconcentration; cow's milk; dioxin; deposition; vapor adsorption

INTRODUCTION

Food is generally recognized as the major exposure route of humans to PCDD and PCDF, with dairy products a major concern. Estimation of such exposure based on air or soil concentrations of PCDD and PCDF has, however, suffered from large uncertainties. First, a number of different models have been proposed for this task. Five recent papers have analyzed the air to cow's milk pathway for 2,3,7,8-TCDD (Connett and Webster, 1987; Travis and Hattemer-Frey, 1987; Stevens and Gerbec, 1988; McKone and Ryan, 1989; Michaels, 1989). Another paper was received too recently for analysis here (Fries and Paustenbach, 1990). Each model includes a different combination of subpathways, summarized in Table i. Each model also uses a different set of parameters. Some of these parameters have not been validated for these compounds with field data, but were extrapolated from other applications.

Furthermore, a recent analysis calculated the uncertainty in such models using Monte Carlo techniques (McKone and Ryan, 1989). The 90% confidence range for exposure to 2,3,7,8-TCDD via dairy products spanned two to three orders of magnitude. Bioconcentration factors (BCFs) and deposition velocity were identified as the major sources of uncertainty.

The best way to resolve such uncertainties lies in the validation of environmental fate models with field data. The use of empirical bioconcentration factors can also be assessed by comparing the situation being modelled with the conditions in the experiment used to determine the BCF. We will use these two techniques to analyze the five models with respect to 2,3,7,8-TCDD. Applicability to 2,3,7,8-TCDD equivalents is also discussed.

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Table i. Factors Considered in Five Models for Estimating the Contribution of Airborne 2,3,7,8-TCDD to Cow's Milk

Model

Direct Deposition Soil Soil Plant to Plants to Plant Ingestion Ingestion Inhalation

Michaels Negl. X - X

Connett & Webster X Negl. - X

Travis & Hattemer-Frey a X X X X

Stevens & Gerbec X Negl. X X

McKone & Ryan X X X X

X

X

X=included in model; -=not included; Negl.=assumed negligible a. Also includes a negligible exposure via water

General Model of the Air to Cow's Milk Pathway

All five models fit within a common framework. Dairy cattle are exposed to atmospheric pollutants by ingestion of contaminated feed, soil, water (negligible), and inhalation of ambient air. This is modelled as:

dep = Ca*V d + wet deposition (i)

Cp = r*dep/(Y*kl)*(l-exp(-kl*t)) + BCFp*C s (2)

C m = BCFmf/Q*f*(ap*Cp*Qp+as*Cs*Qs+aa*Ca*Qa) (3)

Parameters are defined at the end of this paper. Modelling of the concentration in soil is beyond the scope of this paper and will be treated as an exogenous assumption in the remainder of our discussion. Contamination of feed occurs via two processes. The first term in (2) describes direct deposition. The second term estimates concentrations in feed contaminated via all routes from soil--root uptake and translocation, volatilization, resuspension of dust--using an empirically derived BCF n. BCF n should predict the concentration in the above-ground parts of feed pl~nts eaten by cows. The quantity BCFmf/Q*f in (3)--commonly referred to as a biotransfer factor (Fm)--gives concentration in milk as a function of intake. (See Connett and Webster, 1987, for a more complete description of the model).

ComDarison with Backaround Data

The true test of such models is a comparison with field data. Hattemer-Frey and Travis (1989) state that their model has been "verified by empirical studi~s." Assu~ing background levels ~f 2,3,~,8-TCDD in air of 2.2xi0 -16 mol/m ° (70 fg/m ~) and soil of 6.85xi0 -= mol/m ~ (1.5 pg/g), they predicted concentrations in cow's milk of 0.04 pg/g. This result was compared to background levels of 0.01 and 0.03 pg/g measured by Beck et al. (1987) and Rappe et al. (1987).

The cited data may not ~alidate the model. The concentration used for background air (70 fg/m~), referenced to Eitzer and Hites (1986), appears to be a value for total TCDD, not 2,3,7,8-TCDD. More recent work by Eitzer and Hites (1989) in the same cit~, Bloomington, Indiana, resulted in an average total TCDD level of 1.5 fg/m . Air samples ~rom a rural area of Wisconsin showed total TCDD concentrations of 0.3 fg/m ~ (Edgerton, et al. 1989). The

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background air concentration of 2,3,7,8-TCDD experienced by dairy cows has not yet been measured. The concentrations in milk cited by Hattemer-Frey and Travis may not represent a true background. Beck et al. (1987) found 2,3,7,8-TCDD at 0.33 pg/g (fat basis) in one sample. Seven other samples were at or below the detection limit of 0.2 pg/g (fat basis). Rappe et al. (1987) took two samples within I km of municipal incinerators and one about 1 km from a chlorinated chemical industry plant. While the geometric average of these three samples is about 0.03 pg/g, 2,3,7,8-TCDD was not detected in three other samples, two of them pooled controls (DL=0.012-0.013 pg/g). Better background data are required before this approach can be used to validate models.

Comparison with Field Data

Field data have been taken near a copper wire reclamation plant in Brixlegg, Austria. Riss et al. (1988, 1989a, 1989b) measured PCDD and PCDF in soil, hay and milk samples from the same farm situated 1400-2200 m downwind of the plant. The milk was sampled from about twenty cows on the farm fed "almost exclusively with hay from that area;" the amount of cereals added to the diet was only 1-2 kg/day. These data are readily comparable.

Christmann et al. (1989) sampled air 250-300 m downwind, a distance thought to correspond to high soil concentrations. Four samples were taken, each covering two weeks between February and July 1988. Only Sample I is used here, as cable sheathings (presumably PVC) were removed in the latter three, resulting in decreased emissions. The differences in location and date of the air samples--the hay was grown in 1987--make use of these data more problematic. However, this uncertainty is mitigated somewhat by other measurements made by Riss et al. (1988). Concentrations of total TCDD (and other homologues) in grass varied by only about a factor of two over the distance 285-2900 m. Concentrations of 2,3,7,8-TCDD equivalents (dry weight) in hay samples from 1987 were within a factor of two of grass samples from 1988.

Because of these problems, conclusions drawn from these data are suggestive, rather than definitive. Nevertheless, they are the only field data available at this time and we will use them as an order of magnitude check on the five models. Assuming a concentration of 0.i pg/m 3 of 2,3,7,8-TCDD in air (Sample I, Christmann et al., 1989) and about 2 pg/g in soil (Riss et al., 1988), Table 2 shows the predicted concentrations of 2,3,7,8-TCDD in hay and milk fat. These data suggest that only one model underpredicts levels in both hay and milk by more than a factor of ten.

For purposes of comparison with the other models, Tables 2-4 are computed using the expected values for parameters listed by McKone and Ryan (1989). As they point out, such use of expected values can generate exposure estimates significantly less than the expected value computed using Monte Carlo techniques.

Air and Soil to Plant

The major distinction between the five models lies in the transfer of 2,3,7,8-TCDD from air or soil to plants. This is primarily due to the different treatment of direct deposition.

The lowest estimates of hay and milk contamination in Table 2 come from Michaels' (1989) model which, unlike the others, excludes explicit estimation of direct deposition. Michaels estimated BCF D using a set of data that included root crops. Since roots bioconcentr~te 2,3,7,8-TCDD more readily than the above-ground parts of plants, Michaels argued that his BCF D provides a safety factor of at least two that accounts for other pathways such as direct deposition. The Brixlegg data show that bioconcentration from soil cannot account for the 2,3,7,8-TCDD levels found in hay. The concentration in hay divided by the concentration in soil is 4.7, much greater than the range of BCFp values assumed by the models: 0.003-0.03. Hence, indirect

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Table 2. Measured and Predicted Concentrations of 2,3,7,8-TCDD in Dry Hay and Milk Fat (pg/g)a

Connett Stevens Travis & McKone Measured b Michaels & Webster & Gerbec Hattemer-Frey & Ryan c

dry hay 9.4 0.06 d 4.2 0.94 0.17 3.4

milk fat 15.7 0.3 17 e 5.7 f 1.6 g 23g

a. Assume Ca=0.1 pg/m 3, Cs=2 pg/g. b. Brixlegg data from Riss et al. (1988, 1989b). c. Product of expected values of parameters. d. Moisture not specified. A correction factor would depend on the

moisture content of the plant used in the BCF_ experiment. e. Computed with BCFmf, assuming the cow consume~ only hay. f. Computed assuming all exposed feed is hay/grass, milk fat=4%. g. Computed with a biotransfer factor, assuming a mixed diet. NOTE: The field BCFmf=I.7

Table 3. Air/Soil to Fodder Parameters

Connett Stevens Travis & McKone Parameter Michaels & Webster & Gerbec Hattemer-Frey & Ryan a

V d (cm/s) 1.36 b 1 0.3 0.23 0.58 c

r/Y (m2/kg) hay - 2.4 1.8 - - mixed feed - 1.2 0.64 0.4 2.1

k I (d -1) - 0.0495 0.05 0.049 0.039

BCFp 0.03 negl. negl. 0.003 0.03

% deposition d 0 i00 i00 96 98

a. Expected values b. Estimated from Michaels (1989) c. Not strictly comparable as r and wet deposition are included. d. Percent of Cp due to direct deposition with Ca=0.1 pg/m 3 and Cs=2 pg/g.

contamination via soil is probably negligible compared to direct contamination from the air. Indeed, given the concentrations assumed for air and soil in Table 3, the two models that include both pathways estimate that direct deposition is much larger than bioconcentration. The predominance of contamination from the air rather than from soil is suggested by Riss and Hagenmaier (1989) who noted that the homologue pattern found in grass matches ambient air more closely than soil.

In addition to comparison with field data, assumptions made in risk assessments about bioconcentration factors can be judged in another way. In order for an empirical BCF D to predict field conditions, the experiments should include all important processes found in the field. The experiments cited by Michaels (1989) involved plants growing in contaminated soil, rather than plants exposed to deposition (continuous or repeated) from the air, as would occur in the air to cow's milk scenario. Given this crucial omission, it is not surprising that the model underpredicts concentrations in hay and milk.

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Although the direct deposition model matches the field data much better than bioconcentration from soil, Table 2 indicates that this approach may also underpredict levels of 2,3,7,8-TCDD in hay. The discrepancy might be due to the uncertainties in the field data mentioned earlier, but it could also be due to error or uncertainty in the deposition model. Deposition velocity (Vd) is a major source of uncertainty (Webster and Connett, 1989; McKone and Ryan, 1989). McVeety and Hites (1988) recently measured a value of 0.99 cm/sec for aerosol-bound PAH depositing onto a remote lake. The factor r/Y depends on local agricultural yields not specified for Brixlegg. Connett and Webster (1987) and Stevens and Gerbec (1988) assumed values for northern New York State and Minnesota respectively. Furthermore, although the factor k 1 was similar in the four direct deposition models, it is based on physical weathering of other pollutants from plant surfaces.

In addition, all of the models reviewed here assume deposition of particulate-bound 2,3,7,8-TCDD. Eitzer and Hites (1989) indicate that a substantial fraction of TCDD will be in the vapor phase. This suggests that an additional pathway for contamination of feed needs to be taken into account: direct adsorption of vapor from the air. Reischl et al. (1989) estimated partition factors for air to spruce needles for total TCDD of about 25000 and'43000 (w/w) using two regression models. The concentrations of total TCDD in recent spruce needles from Brixlegg appears to be within a factor of two of grass sampled at similar distances (Riss et al., 1988). Application of Reischl's partition factors to the assumed Brixlegg air concentration results in 2,3,7,8-TCDD concentrations in dry hay of 2.1-3.6 pg/g. Although dependent on a number of assumptions which require further study, this alternative model appears to explain the field data as well as the more traditional deposition model. A combination of the particulate deposition and vapor adsorption models may be appropriate. Such a model would include a vapor/particulate partition factor that depends on ambient temperature and the vapor pressure of a compound (Eitzer and Hites, 1989).

Plant to Cow's Milk

The dominant route of exposure for Brixlegg cows is probably ingestion of fodder, not inhalation or ingestion of soil (See Table 4). Soil ingestion would be more significant in the case of a toxic waste site, where soil was the source of contamination rather than air.

Revealing differences between the five models lie in the derivations of the plant to cow's milk bioconcentration factors:

i) Michaels (1989) chose a BCFmf for 2,3,7,8-TCDD based on values of four for beef cattle (Jensen et al., 1981) and five for similar compounds in dairy cattle (Fries, 1987). However, Jensen et al. (1981) estimated a steady-state value of 25 for beef cattle.

2) Connett and Webster (1987) calculated a steady-state BCFmf of 12 for dairy cattle from Jensen and Hummel's data (1982). We reasoned, based on experiments with rats, that the bioavailability of 2,3,7,8-TCDD attached to fly ash in cow's feed would be about one third of that in Jensen and Hummel's (1982) experiment in which 2,4,5-T was added directly to feed.

3) Stevens and Gerbec (1988) calculated the fraction of ingested dose transferred to milk based on Jensen and Hummel (1982), correcting to steady- state. Bioavailability was estimated at 0.4

4) Travis and Hattemer-Frey (1987) estimated their transfer factor with a regression equation based on octanol-water partition coefficients (Kow) . This relatively uncertain value was used despite the fact that Travis and Arms (1988) constructed the regression equation using an experimental value for 2,3,7,8-TCDD. The latter, derived from Jensen and Hummel (1982), was not steady-state.

5) McKone and Ryan (1989) relied on the empirical transfer factor for dairy cattle listed by Travis and Arms (1988) to compute the expected value listed in Table 4.

These assumptions may be judged by their compatability with the field conditions. Steady-state bioconcentration factors should be used since exposure is much longer than the 41 day halflife of 2,3,7,8-TCDD in lactating

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Table 4. Fodder to Cow's Milk Parameters

Connett Stevens Travis & McKone Parameter Michaels & Webster & Gerbec Hattemer-Frey & Ryan a

BCFmf 5 12 NA 25 b 6.8 b

ap 1 0.33 0.4 1 1

f 0.04 0.04 NA 0.0368 0.05

F m (d/kg) - 0.027 c 0.026 c,d 0.058 0.02

Qp (kg/d) exposed - ii 23.1 5 17 total 18 27.6 16 17

Qs (kg/d) - - 0.14 0.i 0.46

% feed e i00 i00 99 81 98

a. Expected values b. Estimated via BCFmf = Fm*Qn/f c Multiply by the relative bioavailability factor (aD~ for field use. d Computed from Stevens and Gerbec (1988) based on their estimate of

40% of daily dose translocated to 15.6 1/day of milk. Since milk fat content was not specified, we have not estimated the BCFmf.

e. Percent of Cmf due to feed assuming Ca=0.1 pg/m 3 and Cs=2 pg/g. NOTE: Inhalation negligible in all cases

dairy cows (Jensen and Hummel, 1982). Since lactation is an efficient means of excretion, data from dairy cattle are preferrable to data from beef cattle. A reduction of bioavailability relative to experiments is probably needed for 2,3,7,8-TCDD bound to fly ash and soil; data on the bioavailability of adsorbed vapor are not available. Compound-specific experimental data are generally preferrable to estimates for a number of reasons: i) possible non-linearities, real or experimental, in the relationship between BCF and Kow; 2) metabolism can depend on factors other than Kow (e.g., whether PCDDs or PCDFs are 2,3,7,8-substituted or not); 3) poorly known Kow values; 4) increased uncertainty when estimating values near the upper end of the data used in the regression.

The apparent field BCFmf is about 1.7 (Table 2), a value lower than that assumed by all of the models. Possible explanations include uncertainty in the field data, variability between cows (Connett and Webster, 1987) and a relative bioavailability lower than 33%. In addition, the feed weights in Jensen and Hummel (1982) were probably wet weight rather than dry weight (Hummel, 1990). Use of a BCFmf based on wet weight would overestimate the concentrations in milk fat when applied to dry hay. McLachlan et al. (1989) estimated 35% transfer of daily dose to milk, corresponding to a field biotransfer factor (aD*Fm) of 0.01, nearly identical to the values assumed by Connett and Webster (1987) and Stevens and Gerbec (1988).

Implications for Modellinq of 2,3,7,8-TCDD Equivalents

Although the bioconcentration factors used in all five models are based on experiments with 2,3,7,8-TCDD, such models are commonly applied to 2,3,7,8- TCDD equivalents. Since the properties of the congeners vary, such an assumption may not be warranted. Choice of 2,3,7,8-TCDD equivalence method is important as well, since congeners which are not 2,3,7,8-substituted tend not to bioaccumulate. Application of the so-called International factors (Safe, 1989) to the Brixlegg data (Christmann et al., 1989; Riss et al.,

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Table 5. Comparison of 2,3,7,8-TCDD and 2,3,7,8-TCDD Equivalent (International) Concentrations

C C C m CD/C a BCFmf Cmf/C a (pg~m3) (pg~g) (pg~g) (~3/g) (w/w) (m3/g)

2378-TCDD 0.i 9.4 15.7 94 1.7 157

TE 1.6 33 49 20 1.5 30

Note: Cp refers to dry hay concentrations. TE = 2,3,7,8-TCDD equivalents

1989b) generates the results in Table 5 (Riss et al., 1988 use the German TE system with different results) The empirically derived BCF_= for TE (1.5) is about 90% of the value for 2 . ,,,L ,3,7,8-TCDD (1.7). Blotransfer of TE is about 60% of 2,3,7,8-TCDD in McLachlan et al. (1989). Comparison of the concentrations in dry hay relative to air (Cp/Ca), suggest that 2,3,7,8-TCDD may be more efficently transferred to hay (or retained) than many congeners. This appears contrary to expectation (Reischl et al., 1989). Overall, reliance on 2,3,7,8-TCDD data alone may overpredict concentrations of 2,3,7,8-TCDD equivalents in cows milk.

CONCLUSIONS

A comparison of field data with estimates of 2,3,7,8-TCDD concentrations in hay and milk show that models which only examine bioconcentration from soil are inadequate. Direct deposition, and possibly vapor adsorption, should be included. The experiments from which bioconcentration factors are derived must be relevant to the application of the health risk assessment. Laboratory and field data will help reduce the large uncertainty in exposure assessment. Given the high degree of bioconcentration of 2,3,7,8-TCDD and related compounds, caution should be exercised in siting new emissions sources in dairy country.

DEFINITIONS OF SYMBOLS

dep = deposition C a =concentration in air V d = deposition velocity C s =concentration in soil r = interception fraction Cp =concentration in fodder Y = yield Cmf =concentration in milk fat k I = leaf rate constant Qa =inhalation by cow f = fat content of milk Qs =soil ingestion by cow BCFp = soil to dry fodder ~ =fodder ingestion by cow

bioconentration factor ~P =ingestion in BCF experiment BCFmf= dry fodder to milk fat a a =air relative bioavailability

bioconcentration factor a s =soil relative bioavailability t = growing time of crop ap =feed relative bioavailability

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