Biological Uptake and Transfer of

Polychlorinated Dibenzo-p-dioxins and

Dibenzofurans

MI C H A E L S. Mc LA C H L A N

1 Introduction
Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) have over the
last 15 years been the subject of intense environmental chemistry research. This
interest is rooted in the persistence and hydrophobicity of these compounds,
which impart to them a strong tendency to bioaccumulate. This, coupled with the
fact that a number of PCDD/Fs have been found to be toxic at very low
concentrations, has fuelled interest in understanding their behaviour in the
environment. One crucial component of the environmental behaviour is the
biological uptake and transfer of PCDD/Fs, since this determines the exposure of
biota to these compounds.
There are 135 chlorinated dibenzofuran and 75 dibenzo-p-dioxin congeners.
The research to date has concentrated on the tetra- to octachlorinated
compounds, since PCDD/Fs with less than four chlorine atoms are not found in
human tissue. Of particular toxicological relevance are the 2,3,7,8-substituted
congeners, of which there are 17. In order to simplify the interpretation of
PCDD/F data, a system known as toxicity equivalents was developed to express
the toxicity of all PCDD/Fs in a sample in terms of the most toxic member of this
family, 2,3,7,8-Cl DD.1
4
A good deal of the concern surrounding this class of compounds has arisen
from the proximity of current background levels of human exposure to the
exposure levels at which toxic effects are suspected. It has been demonstrated that
this background exposure is due almost exclusively to the ingestion of animal fat,
the average uptake in Europe and North America being approximately equally
divided between fish, meat and dairy products (see Table 1).2—5 Owing to the
1 F. W. Kutz, D. G. Barnes, D. P. Bottimore, H. Greim and E. W. Bretthauer, Chemosphere, 1990, 20, 751.
2 P. Fürst, C. Fürst and W. Groebel, Chemosphere, 1990, 20, 787.
3 R. M. C. Theelen, A. K. D. Liem, W. Slob and J. H. van Wijnen, Chemosphere, 1993, 27, 1625.
4 Ministry of Agriculture, Fisheries and Food, Dioxins in Food; Food Surveillance Paper No. 31
HMSO, London, 1992.
5 B. Birmingham, A. Gilman, D. Grant, J. Salminen, M. Boddington, et al., Chemosphere, 1989, 19, 637.

31
 M. S. McLachlan

Table 1 Sources of Country Milk products Meat/eggs Fish products Other Source
human exposure to
PCDD/Fs (in %) Germany 31.5 32.2 31.7 4.5 Ref 2
The Netherlands 42.6 24.6 31.1 1.7 Ref 3
Great Britain 28 34.3 21.4 16.2 Ref 4
Canada 22.2 43.7 12.1 21.9 Ref 5

pre-eminent importance of agricultural products for human exposure, this paper

will focus on bioaccumulation of PCDD/Fs in agricultural food chains. A large
fraction of the PCDD/F exposure through meat is due to beef consumption, and
beef and dairy cattle together account for about one half of human exposure.
Cattle for their part obtain most of their PCDD/Fs through grass.6 Hence the
grass—cattle—milk/beef pathway is critical for human exposure and will receive
special emphasis.
This chapter begins at the bottom of the agricultural food chain, looking at the
uptake of PCDD/Fs in plants from soil. The second section deals with the uptake
in plants from the atmosphere. The attention then switches to the next link in the
food chain, and the transfer from plants and soil to livestock and animal food
products is examined. This is followed by a discussion of uptake in humans from
food and in infants from mothers’ milk. The chapter concludes with a short
summary, an overall perspective on bioaccumulation in the agricultural food
chain, and a brief reference to some consequences of this knowledge for risk
assessment.

2 Soil/Plant Transfer
There are two possible sources of PCDD/Fs to vegetation: the atmosphere and
soil. Initially it was thought that PCDD/Fs would not be present in the
atmosphere in quantities sufficient to contaminate plants owing to their low
volatility, and early research in this area focused on uptake from soil. There are
three possible pathways of soil-bound PCDD/Fs to aerial plant parts: root
uptake and translocation, volatilization followed by adsorption to foliage, and
transfer of soil particles (see Figure 1). The first of these pathways has received the
most attention.

Root Uptake and Translocation

An early paper by Isensee and Jones7 concluded, on the basis of experiments with
radioactively labelled 2,3,7,8-Cl DD, that uptake from soil and translocation to
4
aerial plant parts was unlikely. However, when elevated levels of 2,3,7,8-Cl DD
4
were found in vegetation from the Seveso area that had begun growing one year
after an accident which released large quantities of this compound into the
environment, this was interpreted as evidence of uptake and translocation from
the contaminated soil.8 A second group of researchers analysed vegetation
samples from the same site and came to the opposite conclusion, suggesting that
6 M. S. McLachlan and O. Hutzinger, Organohalogen Compd., 1990, 1, 479.
7 A. R. Isensee and G. E. Jones, J. Agric. Food Chem., 1971, 19, 1210.
8 S. Cocucci, F. Di Gerolamo, A. Verderio, A. Cavallaro, G. Colli, et al., Experientia, 1979, 35, 482.

32
 Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans
Figure 1 Pathways of
PCDD/Fs to plants

the contamination with 2,3,7,8-Cl DD was due to atmospheric deposition and

4
not root uptake/translocation.9 Two research groups then conducted laboratory
experiments growing bean and maize plants in media containing 2,3,7,8-Cl DD.
4
While the first group identified vaporization from soil and subsequent deposition
on leaves as one transport pathway, they concluded that root uptake/translocation
was a much more important mechanism.10 The second group observed that the
leaf concentrations did not increase with time or soil concentration when the
plants were grown in the same atmosphere and concluded that root up-
take/translocation was less significant than volatilization and subsequent
deposition.11 This highly contradictory literature has been reviewed in detail.12
A major reason for the contradictions in this early literature is that in all
experiments both root uptake/translocation as well as volatilization from soil
followed by deposition to the leaf surface were possible. The authors used

9 H.-K. Wipf, E. Homberger, N. Neuner, U. B. Ranalder, W. Vetter, et al., in Chlorinated Dioxins and
Related Compounds: Impact on the Environment, ed. O. Hutzinger et al., Pergamon Press, New
York, 1982, p. 115.
10 G. A. Sacchi, P. Vigano, G. Fortunati and S. M. Cocucci, Experientia, 1986, 42, 586.
11 S. Facchetti, A. Balasso, C. Fichtner, G. Frare, A. Leoni, et al., Chemosphere, 1986, 15, 1387.
12 G. A. Kew, J. L. Schaum, P. White and T. T. Evans, Chemosphere, 1989, 18, 1313.

33
M. S. McLachlan

circumstantial evidence to evaluate the relative importance of the two pathways

and came to different conclusions. This problem was finally overcome with an
experimental apparatus which successfully excluded the volatilization/deposition
pathway.13 Also working with bean and maize, the authors clearly showed that
uptake from soil followed by translocation to aerial plant parts was negligible.
This result is in agreement with what one would expect from very hydrophobic
compounds such as the PCDD/Fs on the basis of current understanding of the
transport of xenobiotics in plants.14 It is also consistent with the subsequent
literature, in which all authors come to the conclusion that the soil uptake/
translocation pathway is insignificant15—20.
An exception to this rule has, however, been discovered: plants of the genus
Cucurbita readily take up and translocate PCDD/Fs from the soil to the leaves
and fruit.21 It is suspected that these plants produce root exudates which form a
complex with PCDD/Fs that is then reabsorbed and transported in the xylem
throughout the whole plant.22,23

Volatilization from Soil/Adsorption to Foliage

Having shown that root uptake/translocation is an insignificant pathway, the
implication of many of the laboratory studies cited above is that volatilization
from soil and subsequent adsorption on aerial plant parts is an important uptake
mechanism. However, using a mathematical model of this process it was shown
that in the field only the lowest few centimetres of plant material would be
contaminated if volatilization occurred.24
This model also indicated that the degree of transfer to aerial plant parts
should decrease with increasing degree of chlorination (decreasing vapour
pressure) of the compound.24 This preferential transfer of the lower chlorinated
congeners was demonstrated in an experiment growing grass on contaminated
soil in a chamber with a low ventilation rate.25 However, in those cases where
aerial parts of plants grown under natural conditions on highly contaminated
soils have been analysed, the pattern of PCDD/Fs found in the plants has been
similar to the pattern present in the soil.16,18 This indicates that the
volatilization/adsorption pathway is not significant, since in this case the pattern
13 J. K. McCrady, C. McFarlane and L. K. Gander, Chemosphere, 1990, 21, 359.
14 G. G. Briggs, R. H. Bromilow and A. A. Evans, Pestic. Sci., 1982, 13, 495.
15 R. Schroll and I. Scheunert, Chemosphere, 1993, 26, 1631.
16 A. Hülster and H. Marschner, Chemosphere, 1993, 27, 439.
17 J. F. Müller, A. Hülster, O. Päpke, M. Ball and H. Marschner, Chemosphere, 1993, 27, 195.
18 G. H. M. Krause, T. Delschen, P. Fürst and D. Hein, UWSF - Z. Umweltchem. Ökotox., 1993, 5, 194.
19 K. Welsch-Pausch, M. S. McLachlan and G. Umlauf, Environ. Sci. Technol., 1995, 29, 1090.
20 G. H. M. Krause, B. Prinz and L. Radermacher, in Kriterien zur Beurteilung organischer
Bodenkontaminationen: Dioxine (PCDD/F) und Phthalate, ed. G. Kreysa and J. Wiesner, Dechema,
Frankfurt a. M., 1995, p. 287.
21 A. Hülster, J. F. Müller and H. Marschner, Environ. Sci. Technol., 1994, 28, 1110.
22 A. Hülster and H. Marschner, Organohalogen Compd., 1994, 20, 31.
23 A. Hülster and H. Marschner, Organohalogen Compd., 1995, 24, 493.
24 S. Trapp and M. Matthies, UWSF - Z. Umweltchem. Ökotox., 1994, 6, 157.
25 G. H. M. Krause, in Aus der Tätigkeit der LIS 1992, Landesanstalt für Immissionsschutz NRW,
Essen, 1993, p. 69.

34
Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans

in the plant would have had a much stronger contribution from the lower
chlorinated homologues than the pattern in the soil.

Transfer of Soil Particles to Foliage

Having excluded soil uptake/translocation and volatilization/adsorption, it can
be concluded that the direct transfer of soil particles is the primary pathway of
PCDD/Fs in soil to aerial plant parts under environmental conditions. This
mechanism is consistent with the similar homologue patterns found in highly
contaminated soils and plants grown on them. The degree of transfer of soil
particles is a function of many variables, including the plant species, the soil
properties and the climate. This transfer is often described using transfer factors
defined as the quotient of the concentrations in the vegetation and the soil, both on
a dry weight basis. Transfer factors of less than 0.001 were measured for PCDD/Fs
in lettuce, potato shoots and hay grown on contaminated soil.16 Transfer factors of
less than 0.01 were reported for hay and garden vegetables from a wide range of
different sites, whereby the authors make the point that their estimates are upper
limits since the concentrations in the vegetation were not corrected for the input
from aerial deposition.20 On the basis of these results it can be concluded that the
soil/vegetation transfer factor is very low for garden vegetables.
This is also true for root vegetables. In field studies it has been found that the
transfer factors for root vegetables are similar to or even lower than those for
aerial vegetation.16,26 It has also been demonstrated that the PCDD/Fs remain
primarily on the surface, not penetrating into root vegetables and fruit.16,17 Since
the PCDD/Fs are transferred via soil particles, washing the vegetables serves to
reduce the PCDD/F concentrations.16
Hay and other fodder crops are more subject to soil contamination. In addition
to natural processes like wind and splash, fodder crops are often contaminated
with soil during harvesting. Since most crops such as hay are not washed prior to
feeding, livestock may ingest considerable quantities of soil. For instance, it was
estimated that in the Netherlands the soil content of grass silage was several
percent.27 This is much higher than the 00.1% reported for manually harvested
grass and vegetables cited above,16 and was calculated to result in an average soil
ingestion rate of 400 g d~1 for milk cows during winter feeding. Root crops such
as fodder beets can be an even more significant source of soil to livestock. The
degree of feed contamination will again be a function of many variables including
soil, climate, crop and harvesting technique. There has been little study in this
area to date, although this is the most important vector of soil-bound PCDD/Fs
into the agricultural food chain.

Summary
In summary, root uptake/translocation is an insignificant pathway of PCDD/Fs
to aerial plant parts, the only known exceptions being several members of the
26 B. Prinz, G. H. M. Krause and L. Radermacher, Chemosphere, 1991, 23, 1743.
27 P. L. M. Berende, Grondopname door melkkoeien, Institute for Livestock Feeding and Nutrition
Research, Internal Report No. 312, Lelystad, 1990.

35
M. S. McLachlan

genus Cucurbita. PCDD/Fs adsorb to the surfaces of root vegetables, but only a
very small fraction is transported deeper into the root tissue. Volatilization
followed by deposition to aerial leaf parts is also of secondary importance under
natural conditions. The main pathway of PCDD/Fs in soil into foliage is the
direct transport of soil particles to the surface of the leaves and fruits. The
soil/plant transfer rates are very low, estimated to be less than 0.001, and much of
this contamination can be removed by cleaning. Of more concern is the
contamination of animal feed with soil, both because the harvesting of feed crops
often is accompanied by the entrainment of considerable quantities of soil, and
because many feed crops are not washed prior to feeding. However, as the next
section shows, all soil-related sources of PCDD/Fs to the agricultural food chain
are small compared to the atmospheric sources.

3 Atmosphere/Plant Transfer
As a consequence of the preoccupation of the dioxin research community with
soil as a source of plant contamination, the investigation of atmospheric
deposition began at a late date. In 1990 it was reported that the concentrations of
PCDD/Fs in grass and in soil growing in a rural area in Central Europe were
similar. If soil was the source of the PCDD/Fs in the grass, this would imply that
the transfer rate was about 1. This is implausible, and the authors concluded that
atmospheric deposition was the source.6 In two other studies, no correlation was
found between the PCDD/F levels in grass and garden vegetables and those in
soil measured at various locations in northwestern Germany, and the authors
came to the same conclusion.20,28 When care was taken to prevent transfer of soil
particles to crops growing on highly contaminated soil in an area with low air
concentrations, the air and not the soil homologue pattern was found in the aerial
plant parts. It was concluded that atmospheric deposition was the primary
source, even when the soil concentrations were very high.16

The Relative Contributions of the Different Forms of Atmospheric

Deposition
Atmospheric deposition of PCDD/Fs can be divided into three different forms:
dry gaseous deposition, dry particle-bound deposition and wet deposition (see
Figure 1). Dry gaseous deposition is the diffusion of gaseous chemicals from the
atmosphere to the plant surface. Dry particle-bound deposition occurs when
particulate matter that contains the contaminant is deposited on the plant
surface. Wet deposition can transport chemicals either in dissolved form, in
particles trapped in the precipitation, or sorbed to the surface of water droplets or
ice crystals. There are a multitude of forms of wet deposition, ranging from hail
through rain to fog and dew fall.
The manner in which a given compound is deposited is determined by the form
in which it is present in the atmosphere. Semi-volatile organic compounds
partition between the gas and particle phases. The lower the vapour pressure of a

28 A. Hembrock-Heger, Organohalogen Compd., 1990, 1, 475.

36
 Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans
Figure 2 Average fraction
of the total air
concentration of the
PCDD/F homologues
that is present in the gas
phase during the summer
months (Data from
ref. 30)

compound, the greater is its tendency to partition onto particles and hence the
greater its likelihood to reach the plant in the form of dry or wet particle-bound
deposition. Similarly, the importance of wet deposition of dissolved chemical is
dependent on its air/water partitioning behaviour. The PCDD/Fs have low
vapour pressures and only a moderate tendency to partition from air into water,
and hence wet deposition of dissolved chemical is of little importance compared
to particle-bound wet deposition. The gas/particle partitioning behaviour during
the growing season is very variable, ranging from almost completely gaseous for
the more volatile Cl DF to virtually completely particle bound for Cl DD (see
4 8
Figure 2).29,30 This makes the determination of the predominant form of
deposition particularly interesting and challenging, since the Cl DF would be
4
expected to be subject to dry gaseous deposition, while in the case of Cl DD wet
8
and dry particle-bound deposition might be expected to dominate.
The first attempts to model PCDD/F accumulation in plants treated only dry
particle-bound deposition.31,32 However, as the research community became
aware of the fact that a large fraction of the toxicologically important lower
chlorinated PCDD/Fs were present in the gas phase during the growing season,
the need to treat other forms of deposition was recognized.6,33 This led to a first
attempt to model all three forms of uptake of 2,3,7,8-Cl DD in grass to see if any
4
of the three forms of atmospheric deposition could be ruled out.34 This modelling
effort revealed the limits of current understanding of the deposition processes,
and the resulting model predictions were at best order-of-magnitude estimates. It
was found that each of the deposition pathways could theoretically by itself
explain the grass concentrations measured in the environment.
An experiment was designed to establish the relative contributions of each of
the different forms of deposition. A system of greenhouses with different exposure
environments was used together with adjacent outdoor plots to study the uptake
of PCDD/Fs in ryegrass. Under the experimental conditions (summer and early
autumn at a semi-rural location in Central Europe) it was found that the uptake

29 M. S. McLachlan and O. Hutzinger, Organohalogen Compd., 1990, 1, 441.

30 M. Hippelein, H. Kaupp, G. Dörr, M. McLachlan and O. Hutzinger, Chemosphere, 1996, 32, 1605.
31 P. Connett and T. Webster, Chemosphere, 1987, 16, 2079.
32 J. B. Stevens and E. N. Gerbec, Risk Anal., 1988, 8, 329.
33 A. Reischl, M. Reissinger, H. Thoma and O. Hutzinger, Chemosphere, 1989, 19, 467.
34 M. S. McLachlan, Organohalogen Compd., 1991, 6, 183.

37
M. S. McLachlan

of the Cl —Cl DD/Fs in the ryegrass was primarily due to dry gaseous deposition.
4 6
The deposition of small particles was not an important pathway for any of the
compounds. No firm conclusions could be drawn for the more strongly particle
associated Cl —Cl DD/Fs, but there were some suggestions that the dry
7 8
deposition of large particles or wet deposition played an important role.19,35
This conclusion was supported by data from field studies. In comparing
homologue patterns in vegetation and in the gaseous and particle phases of the
atmosphere, it was observed that the relative contribution of the lower
chlorinated PCDD/Fs was much higher in vegetation than in particles. It would
only be possible to attribute this to particle-bound deposition if the higher
chlorinated congeners were degraded on the plant surface or if there was a
preferential transfer of lower chlorinated PCDD/Fs from the particles to the
plant followed by erosion of the particles. These explanations were thought to be
unlikely, and the authors concluded that gaseous deposition contributed a large
part of the plant uptake of the Cl —Cl DD/Fs.6,36
4 6
A different interpretation of field data was presented in a third study.26
Vegetation and bulk deposition samples were collected from several locations in
and around the Ruhr industrial region in Germany and analysed. A good
correlation between the PCDD/F concentrations (expressed in toxicity equivalents
(TEQs)) in vegetation and in bulk deposition was observed. On the strength of
this correlation it was concluded that particle-bound deposition is the main
pathway of PCDD/Fs to vegetation. One explanation for the different conclusion
in this study could be that there are more large particles in the air in the Ruhr
area. This would be expected close to combustion sources. Large particles are
deposited quickly and could thus result in a larger contribution of particle-bound
deposition in the Ruhr area than in areas more remote from sources where there
are few large particles in the atmosphere. On the other hand, the data
interpretation in this study does not demonstrate causality. The levels of
PCDD/Fs in bulk deposition and in the gas phase will be correlated, since an
increase in the gaseous concentrations results in an increase in the particle-bound
concentrations through the partitioning phenomenon, hence increasing the bulk
deposition. While a good correlation was obtained between plant levels and bulk
deposition, there is likely an equally good correlation between plant levels and
the gaseous concentrations. The authors could have supported their hypothesis
for the dominant role of particle-bound deposition by showing that the
deposition velocities to the plants calculated with the bulk deposition were
similar for all PCDD/Fs, but they chose to present their data on a TEQ basis only.
The discussion above serves to illustrate that the relative contributions of the
different forms of deposition will be a function of location. Particle-bound
deposition can be expected to be more important where the atmospheric particle
load, particularly for the larger particle sizes, is higher. Similarly, the influence of
wet deposition will depend on the frequency and intensity of precipitation. Plant
characteristics will also be important, with particle-bound deposition playing a
larger role in those plants which are effective at trapping and retaining particles.
Nevertheless, the evidence to date indicates that dry gaseous deposition is the
35 K. Welsch-Pausch, G. Umlauf and M. S. McLachlan, Organohalogen Compd., 1993, 12, 99.
36 G. Rippen and H. Wesp, Organohalogen Compd., 1993, 12, 111.

38
Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans

dominant pathway of the lower chlorinated PCDD/Fs to grass under rural

conditions in Central Europe. Since grass is the main vector of PCDD/Fs into the
human food supply and the lower chlorinated PCDD/Fs are of primary concern
to human health, dry gaseous deposition would appear to be the most important
process.

Dry Gaseous Deposition

Dry gaseous deposition is a partitioning process between the plant and the gas
phase. A simple mathematical model with a plant compartment and an air
compartment can be written to describe this process.37 While there is evidence
that more than one plant compartment is necessary to describe the uptake
behaviour in some species,38 the one compartment assumption would appear to
be reasonable for ryegrass.39 The structure of the model is illustrated in Figure 3.
The defining equations are as follows:

dc
P \ k A(c [ c /K )/V (1)
dt AP A' P PA

where c is the concentration in grass (mol m~3), t is time (h), k is the air/plant
P AP
mass transfer coefficient referenced to the gas phase (m h~1), A is the surface area
of the plant (m2), c is the gaseous concentration in air (mol m~3), V is the plant
A'
volume (m3), and K is the plant/air partitioning coefficient on a volume/volume
PA
basis. k is defined by
AP
1 1 1
\ ] (2)
k k kK
AP A P PA

where k is the mass transfer coefficient from the free atmosphere to the surface of
A
the plant, and k is the mass transfer coefficient from the plant surface to the
P
contaminant reservoir in the plant. The inverse of the mass transfer coefficient is a
resistance, and in the following these two terms will be referred to as the air-side
and plant-side resistances.
For a given plant and a given gaseous concentration there are three unknowns
in this model: the air-side resistance, the plant-side resistance and the plant/air
partition coefficient. There is little information in the literature on the magnitudes
of these parameters for agricultural plants. The one exception is ryegrass, an
important pasture grass for which partition coefficients for a number of
semi-volatile organic compounds (SOCs) have been measured.39 A linear
relationship was proposed to describe the plant/air partition coefficient as a
function of the octanol/air partition coefficient K (see Figure 4):
OA
K \ 0.01 K (3)
PA OA

37 M. S. McLachlan, K. Welsch-Pausch and J. Tolls, Environ. Sci. Technol., 1995, 29, 1989.
38 H. Hauk, G. Umlauf and M. S. McLachlan, Environ. Sci. Technol., 1994, 28, 2372.
39 J. Tolls and M. S. McLachlan, Environ. Sci. Technol., 1994, 28, 159.

39
 M. S. McLachlan
Figure 3 Schematic of a
simple model of air/plant
partitioning

Figure 4 Plot of the

measured plant/air
partitioning coefficient of
several SOCs in ryegrass
as a function of the
octanol/air partition
coefficient (Modified from
ref. 39)

While this equation was obtained for compounds that are somewhat more
volatile than the PCDD/Fs, it is consistent with theoretical models of plant
uptake of SOCs40—43 and it would seem reasonable to extrapolate it to the
PCDD/Fs.
The same authors also measured the plant-side resistance for the same SOCs in
ryegrass. They found no apparent relationship between the magnitude of the
plant-side resistance and the molecular properties.39 This is in agreement with
studies of the plant uptake of SOCs in aqueous systems, where it was found that
the plant-side resistance was relatively independent of the hydrophobicity for
compounds of similar molecular volume.44 The average value for k in ryegrass
P
40 K.-W. Schramm, A. Reischl and O. Hutzinger, Chemosphere, 1987, 16, 2653.
41 M. Riederer, Environ. Sci. Technol., 1990, 24, 829.
42 S. Trapp, M. Matthies, I. Scheunert and E. M. Topp, Environ. Sci. Technol., 1990, 24, 1246.
43 S. Paterson, D. Mackay and A. Gladman, Chemosphere, 1991, 23, 539.
44 H. Bauer and J. Schönherr, Pestic. Sci., 1992, 35, 1.

40
 Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans
Figure 5 Comparison of
measured and modelled
plant/air concentration
quotients for PCBs and
PCDD/Fs as a function of
the octanol/air partition
coefficient (Modified from
ref. 37)

was 2.8 ] 10~6 m h~1 on a whole plant basis.39 Since the SOCs studied in this
work have molecular volumes similar to the PCDD/Fs, this should be a
reasonable estimate for the PCDD/Fs as well.
Having established estimates for two of the three unknowns, the simple model
of dry gaseous deposition shown in Figure 3 was applied to a dataset consisting of
PCB and PCDD/F concentrations from a ryegrass culture that had been grown
outside in flower boxes and from air samples which had been collected during the
growing period.37 The third model parameter, the air-side resistance, was fitted,
and the modelled and measured grass concentrations were compared. The
agreement was excellent, with maximum deviations between the measured and
modelled values of 30% for almost all compounds. Only the Cl —Cl DD/F
7 8
displayed higher deviations, with the model underpredicting the measured
concentrations. This was attributed to particle-bound deposition which was not
accounted for in the model.
In Figure 5 the log of the quotient of the grass and gaseous concentrations for
this experiment is plotted against log K . In the left part of the plot the grass/gas
OA
phase concentration quotients increase linearly with K , indicating partitioning
OA
equilibrium in accordance with equation (3). However, at higher K values the
OA
behaviour changes, and the grass/gas phase concentration quotients reach a
more or less constant value that does not change with increasing K . The
OA
grass/gas phase concentration quotients lie below the equilibrium partitioning
coefficients given by the extension of the curve on the left of the figure. This is
indicative of a non-equilibrium state, and all of the PCDD/Fs lie in this portion of
the plot. This is an important result, since it indicates that the resistance and not
the partition coefficient will determine PCDD/F accumulation in vegetation.
Of the two resistances that limited uptake, the model indicates that the air-side
resistance was dominant.37 Expressed in simple terms, for compounds with
partition coefficients in the order of 107 or more, the plant does not ‘see’ enough
air in its lifetime to allow it to achieve equilibrium. Given this and the fact that the
PCDD/Fs were orders of magnitude away from equilibrium, equation (1) can be
simplified to

41
M. S. McLachlan

dc
P \ k Ac /V (4)
dt A A'

or

P
1
c \ k Ac dt (5)
P V A A'

This states that the concentration of the lower chlorinated PCDD/Fs in

vegetation is the time integral of the product of the air-side mass transfer
coefficient (the inverse of the air-side resistance), the specific surface area of the
vegetation and the gaseous air concentration.
Can this equation be extended to other plant species? While the non-equilibrium
accumulation behaviour has to date only been demonstrated for this ryegrass
culture, it is likely also true for other agricultural plants since the PCDD/Fs in the
ryegrass were orders of magnitude away from equilibrium although the
deposition velocities were higher than under natural conditions due to the
elevated exposure of the flower boxes. It is improbable that the plant-side
resistance could dominate the air-side resistance due to the very high K values
PA
for the PCDD/Fs (see equations 2 and 3). It may be that particle-bound
deposition makes a significant contribution to the levels of lower chlorinated
PCDD/Fs for plants that have much better particle trapping properties than
ryegrass, or under atmospheric conditions with much higher particle-bound
deposition velocities than in Bayreuth where this study was conducted. However,
it is felt that equation (5) will be valid for the Cl —Cl DD/Fs for most agricultural
4 5
crops under most conditions.
The one remaining unknown in equation (5) is the air-side mass transfer
coefficient, which is often referred to as a deposition velocity. It describes the
limitations on the transport of gaseous PCDD/Fs from the free atmosphere to the
surface of the plant. It can be viewed as having two components: a turbulent
resistance describing the transport from the free atmosphere to the laminar
boundary layer surrounding the leaf, and a laminar resistance describing the
transport through the laminar boundary layer to the surface of the cuticle. As a
whole, the deposition velocity is a function of many factors, including the wind
speed, temperature, solar radiation, atmospheric stability, canopy structure and
leaf surface structure. For a given situation it is, however, very similar for all
PCDD/Fs, since it depends only on the diffusivity of the molecule in air.
Diffusivity in air is approximately proportional to the square root of the
molecular weight, and since this varies by only 50% between Cl DF and Cl DD,
4 8
the diffusivity can be expected to vary by less than 25%.
Air-side deposition velocities have been studied extensively for the uptake of
inorganic gases in plants. However, the deposition of PCDD/Fs introduces a new
dimension to this subject, since these compounds are deposited primarily to the
surface of the cuticle,45 not to the stomatal openings as in the case of most
inorganic trace gases. Hence the receptor surface is fundamentally different for

45 A. Reischl, H. Thoma, M. Reissinger and O. Hutzinger, Naturwissenschaften, 1987, 74, 88.

42
Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans

the PCDD/Fs, and the deposition velocities for inorganic gases in the literature
are of limited use for predicting k in equation (5).
A
There is little information in the literature on deposition velocities of
PCDD/Fs or other SOCs to plants. The value measured for the flower box
culture experiment described above cannot be extrapolated to environmental
conditions. The only values the author is aware of were reported for hay and corn
silage grown near to Bayreuth in 1989.46 The data were presented as air
scavenging ratios, the amount of air that 1 g of plant material scavenged during
its lifetime. When the values of 9 m3 g~1 dw and 4.5 m3 g~1 dw for grass and corn
are converted to average deposition velocities, values of 0.0006 m s~1 and
0.00018 m s~1 are obtained. Note that these are deposition velocities to the
canopy, not to the leaf surface, and in this case A in equation (5) has to be defined
as canopy area occupied by the plant and not its surface area. These values
represent first estimates only, and more research is needed to measure deposition
velocities of PCDD/Fs to crops under typical agricultural conditions.
Other interpretations of dry gaseous deposition of PCDD/Fs to plants have
been presented in the literature. In one paper, different plants were placed in a
chamber and exposed to 2,3,7,8-Cl DD.47 The uptake constants were measured
4
and it was found that they correlated well with the specific surface area of the
plant. This is in agreement with equation (5) (assuming that the specific surface
area A/V has no effect on the deposition velocity k under the chamber
A
conditions), but the author attributed his results to a plant-side instead of an
air-side resistance. In an earlier paper this author had used uptake rates and
clearance rates measured under conditions of different turbulence to calculate
plant/gas phase partitioning coefficients for 2,3,7,8-Cl DD.48 This approach and
4
the models that have been developed from it49,50 should be reconsidered in light
of the fact that the uptake and clearance rates are dominated by the air-side
resistance (and hence by the turbulence).

Particle-bound Deposition
As described above, wet and dry particle-bound deposition are likely important
for the accumulation of the higher chlorinated PCDD/Fs in aerial vegetation.
The accumulation of particle-bound PCDD/Fs in plants is a function of a myriad
of factors. The deposition rate itself is influenced by the particle size spectrum in
the atmosphere and the distribution of the PCDD/Fs on the different particle size
fractions, and further by the atmospheric turbulence, the canopy and plant
properties, and the frequency and intensity of precipitation. The retention of the
contaminants on the plant surface depends on the degree to which the particles
are permanently retained on the plant and, for those particles which are not
retained, the degree of transfer of PCDD/Fs from the particles to the plant cuticle.
This is a very complex system that is not yet well understood. One approach that
46 M. S. McLachlan, Organohalogen Compd., 1995, 26, 105.
47 J. K. McCrady, Chemosphere, 1994, 28, 207.
48 J. K. McCrady and S. P. Maggard, Environ. Sci. Technol., 1993, 27, 343.
49 M. Lorber, D. Cleverly, J. Schaum, L. Phillips, G. Schweer, et al., Sci. Total Environ., 1994, 156, 39.
50 M. Lorber, Organohalogen Compd., 1995, 24, 179.

43
M. S. McLachlan

has been taken to predict deposition of PCDD/Fs is to use particle deposition

models and particle erosion models that were developed using radioactive
tracers.32,49 However, the extrapolation of these models to PCDD/Fs can be
questioned since these compounds will be associated with particles having
different sizes and properties than radionuclide particles. A second approach is to
use field data to obtain average long-term net deposition velocities of particle-
bound PCDD/Fs. For corn and hay it was reported that the gaseous deposition
velocities and the net particle bound deposition velocities were very similar (i.e.
0.00016 and 0.0006 m s~1 respectively; see above).46 While these values provide a
first estimate, much remains to be learned about particle-bound deposition of
PCDD/Fs to plants.

Persistence of PCDD/Fs in Plants

The persistence of PCDD/Fs in plants has not been extensively investigated to
date. There is little reason to expect that biodegradation is relevant, given that the
PCDD/Fs are found primarily in the non-viable cuticle and that they are very
resistant to microbial degradation.
There has been one report of photodegradation of 2,3,7,8-Cl DD in reed
4
canarygrass that was exposed to sunlight following gaseous contamination.48
However, in another study, no differences were observed between the PCDD/F
concentrations in two pasture grass cultures exposed to background air levels,
one in the presence of and one protected from UV radiation, which led the
authors to conclude that photodegradation is not relevant under natural
conditions.51 The contradictions between these two studies have yet to be resolved.

Summary
Atmospheric deposition is the dominant source of PCDD/Fs in vegetation. Dry
gaseous deposition is the primary pathway of the lower chlorinated PCDD/Fs to
agricultural plants, while particle-bound deposition is likely a significant
mechanism for the higher chlorinated congeners. Dry gaseous deposition is a
diffusive partitioning process, but in the case of the PCDD/Fs a partitioning
equilibrium is not approached. The uptake is limited by an air-side resistance,
and hence atmospheric turbulence is the primary factor besides the gaseous
concentration and time in determining the concentrations of the lower chlorinated
congeners in vegetation. Particle-bound deposition is a more complex process.
There is some evidence that gaseous and net particle-bound deposition velocities
to plants are similar, but much more work is needed to obtain good estimates of
these parameters.

4 Transfer from Plants to Livestock and Animal Food

Having addressed the accumulation of PCDD/Fs in plants, this section will
discuss the transfer from plants to animals, focusing in particular on cattle. First,

51 K. Welsch-Pausch and M. S. McLachlan, Organohalogen Compd., 1995, 24, 509.

44
Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans

the sources of PCDD/Fs to livestock will be reviewed. Thereafter the persistence

of different congeners in livestock will be examined. This will be followed by a
discussion of plant/animal transfer of PCDD/Fs under steady-state and non-
steady-state conditions. Finally, a simple model of contaminant accumulation in
an agricultural food chain will be discussed.

Sources of PCDD/Fs to Livestock

As was mentioned in the introduction, it has been shown that feed is the primary
source of PCDD/Fs to cattle. Water and air make negligible contributions to
exposure.52 The same can be expected for other livestock, given the very low
vapour pressure and hydrophobic nature of this class of compounds.
Based on the discussion of PCDD/F uptake in plants, it can be expected that
plant components with a large exposed surface area per unit mass will have
higher concentrations of PCDD/Fs and be more important vectors to livestock
than feeds which develop protected from the atmosphere. This was investigated
for the feed ration of cows in Bayreuth and found to be true, with grass products
making the dominant contribution to PCDD/F uptake followed by corn silage,
while concentrate consisting primarily of grain was of little importance.6 The
more pronounced accumulation in leafy plants is reflected in the PCDD/F
concentrations found in different types of meat. Ruminants which consume large
quantities of grass have higher PCDD/F levels than pigs, for instance, which
consume little if any leafy material.53
Another pathway of PCDD/Fs to livestock that has attracted considerable
interest is the direct ingestion of soil by grazing animals. In a recent review it was
emphasized that there has been a tendency to use unrealistically high values for
soil uptake.54 While soil ingestion rates between \1 and 18% have been
measured in sheep and cows, the higher values were associated with winter
grazing and no supplemental feed. It is stated that soil ingestion rates of 1—2% of
dry matter intake are unlikely to be exceeded when modern agricultural practices
involving supplementary feeding are employed, at least in areas where climatic
conditions prevent year-round grazing. In another paper the average soil
ingestion rate of grazing milk cattle in Holland was estimated to be 225 g d~1,
about 1.2% of the total dry feed intake.27 It is interesting to note that this is less
than the same author’s estimate of soil intake in winter from grass silage,
suggesting that the cow is more selective than the harvesting machine.
This soil ingestion rate was used together with an estimate of the background
level of feed contamination in northwestern Germany in 1990 to compare the
relative contributions of soil and feed to uptake of PCDD/Fs by cattle. It was
found that the soil concentration would have to be 47 ng TEQ kg~1 for the
uptake from soil to equal the uptake from feed.34 However, the concentrations of
PCDD/Fs in air are decreasing in Germany.55 This is being accompanied by a
decrease in feed concentrations, which is reflected in the pronounced decrease in
52 M. S. McLachlan, H. Thoma, M. Reissinger and O. Hutzinger, Chemosphere, 1990, 20, 1013.
53 O. Päpke and P. Fürst, Organohalogen Compd., 1995, 22, 143.
54 G. F. Fries, Sci. Total Environ., 1996, 185. 93.
55 E. Hiester, P. Bruckmann, R. Böhm, P. Eynck, A. Gerlach, et al., Organohalogen Compd., 1995, 24, 147.

45
M. S. McLachlan

milk concentrations.56 If this trend continues the relative importance of soil

ingestion and soil contamination of feed as a source of PCDD/Fs to the food
chain will increase. The decrease in feed contamination will have to be close to an
order of magnitude though, before typical agricultural soils (1—5 ng TEQ kg~1)
begin to contribute significantly to contamination of dairy products and
beef.
Soil uptake can have a more significant impact on PCDD/F concentrations in
eggs from free-ranging hens.57,58 In a survey of eggs conducted in northwestern
Germany, eggs from free-ranging hens had considerably higher concentrations
than eggs from hens housed in elevated cages.59 This can be attributed to the high
soil ingestion of foraging hens. While this pathway is of little relevance for the
general food supply in industrialized countries, it can be important for small
sub-populations.

Persistence of PCDD/Fs in Livestock

In general, only 2,3,7,8-substituted PCDD/Fs are found in livestock. The results
of a mass balance of a lactating cow indicated that the non-2,3,7,8-substituted
PCDD/Fs are absorbed from the feed in the digestive tract and then metabolized.52
This study also showed that several of the 2,3,7,8-substituted dibenzofurans are
largely metabolized in cattle, namely 2,3,7,8-Cl DF and 1,2,3,7,8-Cl DF. It is
4 5
suspected that 1,2,3,7,8,9-Cl DF is also metabolized, but the low concentrations
6
of this congener have frustrated the resolution of this question. The metabolism
of 2,3,7,8-Cl DF and 1,2,3,7,8-Cl DF is also apparent from feeding studies in
4 5
which the half-life of these congeners in the cow were orders of magnitude lower
than the half-lives of other 2,3,7,8-substituted PCDD/Fs.60,61 A similar behaviour
has been reported for hens.62

Steady-state Transfer in Livestock

A steady state exists when the uptake, storage and excretion of a substance does
not change with time. Given that the concentrations of PCDD/Fs in feed are
relatively constant, milk cows and egg laying hens are in an approximate
PCDD/F steady state. The one exception is the cow that has calved for the first
time. In this case the PCDD/Fs that it has accumulated as a heifer are initially

56 O. Fürst and K. Wilmers, Organohalogen Compd., 1995, 26, 101.

57 R. R. Chang, D. G. Hayward, L. R. Goldman, M. Harnly, J. J. Flattery, et al., Chemosphere, 1989,
19, 481.
58 R. D. Stephens, M. Harnly, D. G. Hayward, R. R. Chang and J. J. Flattery, Chemosphere, 1990, 20, 1091.
59 P. Fürst, C. Fürst and K. Wilmers, Organohalogen Compd., 1993, 13, 31.
60 M. Olling, H. J. G. M. Derks, P. L. M. Berende, A. K. D. Liem and A. P. J. M. de Jong,
Chemosphere, 1991, 23, 1377.
61 W. Heeschen, A. Blüthgen and U. Ruoff, Untersuchungen zum Übergang ausgewählter polychlorierter
Dibenzo-para-dioxine und-Furane nach oraler Supplementierung in die Milch laktierender Kühe,
Bundesanstalt für Milchforschung, Kiel, 1994.
62 R. D. Stephens, M. X. Petreas, D. G. Hayward, R. R. Chang, L. R. Goldman, et al., poster presented
at the 11th International Symposium on Chlorinated Dioxins and Related Compounds, Research
Triangle Park, 23—27 September, 1991.

46
Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans

excreted through the milk, and a steady state is only approached sometime
during the first lactation period.63
At steady state the excretion of a persistent compound equals the uptake. In
cows and hens, feed/soil is the only relevant source of PCDD/F uptake, and there
are two forms of excretion: faeces and milk/eggs. If, for a given PCDD/F uptake,
the flux in the faeces can be determined, then the net transfer of PCDD/Fs from
the feed to the food product (often referred to as carryover) can be easily
calculated. Or, in other words, at steady state all of the persistent PCDD/Fs that
are absorbed by the animal are transferred to the milk/eggs. Hence, we need to
understand absorption in order to understand carryover.
A mass balance of a lactating cow was conducted to measure absorption of
PCDD/Fs.52,64 It was found that the absorption of the PCDD/Fs decreased
with increasing degree of chlorination. This decrease was attributed to the
increasing hydrophobicity of the PCDD/Fs in a model of contaminant transfer in
the cow.65
While this was the only study that directly investigated absorption, there have
been a number of reports on feed to milk transfer. These are summarized in Table
2 as carryover rates, defined as the fraction of the ingested contaminant that is
excreted in the milk at steady state. The data in the first four papers were obtained
from feeding studies in which cows were fed PCDD/Fs, usually in capsule form,
and the steady-state excretion rate was extrapolated from the uptake and
clearance kinetics.32,60,61,66 The fifth column gives the results of the mass
balance study,64 and the data in the sixth column were obtained from a field
study.67 There is generally good agreement between the studies, the carryover
ranging from about 0.35 for the lower chlorinated persistent congeners down to
several percent at most for Cl DD/F.
8
There is very little information on how the form in which the PCDD/Fs are
present in the feed influences the absorption and hence carryover. Table 2 shows
good agreement between the feeding studies in which the PCDD/Fs were
artificially added to the feed and the mass balance study where the only source of
PCDD/Fs was from naturally contaminated feed from a rural area. However, the
carryover rate and hence the absorption were lower in the field study, which was
conducted near a known source of PCDD/Fs. It was suggested that the lower
carryover in the field study was due to a lower absorption of PCDD/Fs from
flyash that had been deposited on the feed following emission from a nearby
incinerator. This hypothesis was supported with the results of a laboratory study
in which cows were fed PCDD/Fs on fly ash. The carryover in this case was more
than an order of magnitude lower than in the field study.67 This shows that the
source of the PCDD/Fs can influence absorption in the cow. It remains to be seen
whether the carryover of PCDD/Fs in soil, sewage sludge or other specific
63 M. S. McLachlan, in Kriterien zur Beurteilung organischer Bodenkontaminationen: Dioxine
(PCDD/F) und Phthalate, ed. G. Kreysa and J. Wiesner, Dechema, Frankfurt a. M., 1995, p. 309.
64 M. S. McLachlan, Das Verhalten hydrophober chlororganischer Verbindungen in laktierenden
Rindern, Doctoral Thesis, University of Bayreuth, 1992.
65 M. S. McLachlan, Environ. Sci. Technol., 1994, 28, 2407.
66 D. Firestone, M. Clower, Jr., A. P. Borsetti, R. H. Teske and P. E. Long, J. Agric. Food Chem., 1979,
27, 1171.
67 W. Slob, M. Olling, H. J. G. M. Derks and A. P. J. M. de Jong, Chemosphere, 1995, 31, 3827.

47
 M. S. McLachlan

Table 2 Carryover rates of Congener Ref 32 Ref 60 Ref 61 Ref 66 Ref 64 Ref 67
2,3,7,8-substituted
PCDD/Fs from feed to 2,3,7,8-Cl DD 0.40 0.30 0.35—0.60 0.36 0.15
4 DD
1,2,3,7,8-Cl 0.28 0.10—0.15 0.32 0.10
milk 5 DD
1,2,3,4,7,8-Cl 0.05—0.10 0.16 0.06
1,2,3,6,7,8-Cl6DD 0.33 0.27 0.10—0.15 0.15 0.06
1,2,3,7,8,9-Cl6DD 0.05—0.10 0.15 0.03
6 DD
1,2,3,4,6,7,8-Cl 0.03 0.02 0.03 0.006
Cl DD 7 0.01 0.04 0.001
8
2,3,7,8-Cl DF 0.01 \0.01 0.07 0.008
4 DF
1,2,3,7,8-Cl 0.01—0.05 0.05 0.005
2,3,4,7,8-Cl5DF 0.36 0.25—0.35 0.33 0.12
5 DF
1,2,3,4,7,8-Cl 0.18 0.05—0.10 0.15 0.04
1,2,3,6,7,8-Cl6DF 0.15 0.04
2,3,4,6,7,8-Cl6DF 0.14 0.04
6 DF
1,2,3,4,6,7,8-Cl 0.02 \0.01 0.03 0.004
1,2,3,4,7,8,9-Cl7DF 0.08 0.005
Cl DF 7 0.02
8

PCDD/F sources differs considerably from the carryover in ‘naturally’ con-

taminated feed.
There has been considerably less work on steady-state carryover in hens.
However, in one detailed study it was shown that the absorption of PCDD/Fs
from a contaminated soil was quite high, ranging from 70—80% for the
tetrachlorinated congeners to 10% for the octachlorinated ones.68 The authors
compared their results to feeding studies with rodents and came to the conclusion
that absorption from soil was as effective as absorption from easily digestible
carriers such as corn oil.

Non-steady-state Transfer in Livestock

Whereas milk cows and egg laying hens are at a near steady state, animals raised
for meat production such as beef cattle and pigs are not. These animals do not
have the possibility to excrete the PCDD/Fs in a lipid-rich matrix such as milk or
eggs. All of the persistent contaminant that is absorbed is stored in the body.
Although they could theoretically reach a steady state in which the net
absorption of persistent PCDD/Fs was zero, this condition is not approached
under modern animal husbandry practices. The life span of the animals is short
and the growth rate is high, serving constantly to dilute the contaminant stores in
the animal. Indeed, PCDD/F concentrations in beef fat are generally quite similar
to those in milk fat,2,3 although the steady-state concentration in beef cattle has
been estimated to be at least an order of magnitude higher than in lactating cows.65
Several approaches have been used to predict the transfer of persistent organic
contaminants from feed to beef. One involves simply using a bioconcentration or
biotransfer factor, a ratio of the concentration in animal fat to the concentration
or uptake in the feed.49 This method has the disadvantage that it does not
account for variability in animal husbandry practices. A more sophisticated

68 R. D. Stephens, M. X. Petreas and D. G. Hayward, Organohalogen Compd., 1994, 20, 55.

48
Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans

approach that provides detailed information is to conduct a model simulation of

the accumulation in the animal. For instance, it was shown for pigs that the
residue concentration peaks at about 100 days of age and then decreases due to
the shift in energy partitioning from protein deposition to fat deposition with
increasing age.69 Recently, a method has been proposed which is simple but still
accounts for the most important variables. The total amount of a persistent
contaminant ingested by an animal over its lifetime is multiplied by the
absorption rate and divided by the weight of lipid in the animal at slaughter to
obtain the lipid-based concentration.65 This approach makes use of the fact that
the PCDD/Fs are stored almost exclusively in body lipids.
Another aspect of non-steady-state behaviour that is occasionally of interest is
the clearance of a chemical from a contaminated animal. Feeding studies have
shown the clearance from non-lactating cattle to be very slow, with half-lives in
the order of several hundred days.70,71 It is not known if the disappearance is due
to metabolism or other mechanisms. While the loss from the animal is very slow,
the concentrations can decrease as a result of growth dilution.72
Clearance from lactating cows has been studied much more intensively.
Half-lives in the order of 30—60 days have generally been found.60,66,73,74 The
half-life can be expected to increase with increasing body lipid weight and
decreasing lactation rate of the contaminated animal.65 There is evidence of a
rapid initial drop in milk fat concentrations following removal of the contaminant
source from the diet, and this has been described using a pharmacokinetic model.75

A Simple Model of PCDD/F Accumulation in an Agricultural

Food Chain
The knowledge about the uptake of PCDD/Fs by plants was combined with
information on the transfer from feed to animal products to assemble a predictive
model of PCDD/F accumulation in the most important agricultural food chain
for human exposure to these compounds, namely air—fodder—cow—milk.46 The
air/plant scavenging ratios of 9 m3 g~1 dw for grass and 4.5 m3 g~1 dw for corn
silage were multiplied by typical grass and corn silage rations for dairy cows in
Bavaria and added. The resulting number, 100 000, gives the equivalent volume
of air cleaned by the feed that a cow eats daily (i.e. the cow ‘eats’ the PCDD/Fs in
100 000 m3 of air). Multiplying this by the air concentration c (gaseous ] particle
A
bound) yields the daily uptake of the PCDD/F congener by the cow. This is then
multiplied by the carryover rates from the mass balance study (see Table 2) and
69 G. F. Fries, Organohalogen Compd., 1994, 20, 51.
70 D. J. Jensen, R. A. Hummel, N. H. Mahle, C. W. Kocher and H. S. Higgins, J. Agric. Food Chem.,
1981, 29, 265.
71 M. Olling, P. L. M. Berende, H. J. G. M. Derks, A. K. D. Liem, H. Everts, et al., De toxikokinetiek
van PCDD’s en PCDF’s in niet lacterende koeien (vetweiders), Rijksinstituut voor Volksgezondheid
en Milieuhygiene, Rapport 328904003, Bilthoven, 1991.
72 J. R. Startin, C. Wright, M. Kelly and N. Harrison, Organohalogen Compd., 1994, 21, 347.
73 D. J. Jensen and R. A. Hummel, Bull. Environ. Contam. Toxicol., 1982, 29, 440.
74 A. Riss and H. Hagenmaier, VDI Ber., 1991, 901, 863.
75 H. J. G. M. Derks, P. L. M. Berende, M. Olling, H. Everts, A. K. D. Liem, et al., Chemosphere, 1994,
28, 711.

49
M. S. McLachlan

divided by an average daily milk fat lactation rate to give the milk fat
concentration c :
M
c \ c ] 100 000 ] carryover/lactation (g milk fat d~1) (6)
M A
This simple model was tested using data from air samples collected in Bayreuth
during the summer of 1989. The predicted milk concentrations were compared
with the average concentrations obtained in a survey of over 100 milk samples
collected in Bavaria in 1989 and 1990. There was excellent agreement between the
predicted and measured milk concentrations for almost all congeners (see Figure
6). This suggests that there is now a good basic understanding of the
accumulation of these compounds in agricultural food chains.

5 Transfer from Food to Humans

The primary sources of human exposure to PCDD/Fs were outlined in the
introduction. For North America and Western Europe, uptake of these
compounds is about equally divided between dairy, meat and fish products (see
Table 1). The levels in the diet are decreasing in some countries. The most recent
estimates for Germany suggest an intake of 55—70 pg TEQ d~1 for adults.76
Of crucial importance for the potential risk associated with this contamination
of the diet is the question: how much of the ingested PCDD/Fs is actually
absorbed and retained in the body? There is, however, remarkably little in-
formation on this subject. There is one report of absorption in an adult man
where 87% of a single dose of radioactively labelled 2,3,7,8-Cl DD dissolved in
4
corn oil was taken up.77 In another study, in which only faeces samples from two
individuals on an unmodified diet were analysed, it was found that the excretion
rate was very high compared to the theoretical uptake rate,78 which would
suggest that absorption is low. No work beyond these two somewhat contradictory
studies was found.
Of particular interest is the question of whether or not an absorptive steady
state is approached. In this case the net absorption of a compound from the
normal diet would be near zero. Human tissue levels might then be determined
primarily by highly contaminated foods which are seldom consumed but
nevertheless result in a significant absorption of the compound. This would have
dramatic consequences for the way risk analysis is done and the identification of
means to reduce the risk associated with PCDD/Fs.79 There is an urgent need for
more research in this area.
It is known that the PCDD/Fs are very persistent in humans. Half-lives of most
2,3,7,8-substituted congeners have been measured in occupationally exposed
cohorts and found to lie in the range of 5—15 years.80 This results in accumulation
in humans, and the concentrations in human fat are at least an order of
magnitude higher than in cows’ milk fat or beef fat.79 As in livestock, the
76 M. Grün, O. Päpke, M. Weibrodt, A. Lis, M. Ball, et al., Organohalogen Compd., 1995, 26, 151.
77 H. Poiger and C. Schlatter, Chemosphere, 1986, 15, 1489.
78 R. Andersson and C. Rappe, Organohalogen Compd., 1992, 9, 195.
79 M. S. McLachlan, Environ. Sci. Technol., 1996, 30, 252.
80 D. Flesch-Janys, P. Gurn, D. Jung, J. Koonietzko, A. Manz, et al., Organohalogen Compd., 1994, 21, 93.

50
 Biological Uptake and Transfer of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans
Figure 6 Comparison of
the predicted and
measured concentrations
of the 2,3,7,8-substituted
PCDD/F congeners in
milk (Taken from ref. 46)

concentrations of 2,3,7,8-Cl DF and 1,2,3,7,8-Cl DF are very low in humans,

4 5
suggesting that these congeners are metabolized.

6 Transfer from Human Milk to Infants

Nursing infants are exposed to unusually high levels of PCDD/Fs. As their food
source is human milk, they are effectively one link higher in the food chain than
the rest of the population. At the end of the 1980s it was estimated that nursing
infants in developed countries ingest about 85 pg of 2,3,7,8-Cl DD toxicity
4
equivalents (TEQs) per kg body weight and day.81 While there is evidence that
the mothers’ milk concentrations have decreased in the meantime,53,82 infant
exposure is still far in excess of the recommended acceptable daily intakes (ADIs),
which range from 0.0064 to 10 pg TEQ kg~1 BW day, depending on the
jurisdiction.83
In contrast to adults, in nursing infants the absorption of PCDD/Fs has been
well studied. All investigators have come to the same conclusion, namely that the
absorption of PCDD/Fs is nearly complete.84—88. The high exposure of infants
continues to be one of the biggest concerns in the dioxin issue.

7 Concluding Remarks
To review, PCDD/Fs enter the food chain primarily from the atmosphere.
Diffusion of gaseous PCDD/Fs to the lipophilic cuticle is the primary mechanism
of uptake into plants, although the deposition of particle-bound chemical likely
81 WHO, Levels of PCBs, PCDDs, and PCDFs in Breast Milk, WHO Regional Office for Europe,
FADL, Copenhagen, 1989.
82 P. Fürst, C. Fürst and K. Wilmers, Chemosphere, 1992, 25, 1029.
83 E. W. Bretthauer, H. W. Kraus and A. di Domenico, Dioxin Perspectives. A Pilot Study on
InternationalInformationExchangeonDioxins andRelatedCompounds,PlenumPress,NewYork,1991.
84 B. Jödicke, M. Ende, H. Helge and D. Neubert, Chemosphere, 1992, 25, 1061.
85 W. Körner, N. Dawidowsky and H. Hagenmaier, Chemosphere, 1993, 27, 157.
86 H. J. Pluim, J. Wever, J. G. Koppe, J. W. vd Slikke and K. Olie, Chemosphere, 1993, 26, 1947.
87 M. S. McLachlan, Toxicol. Appl. Pharmacol., 1993, 123, 68.
88 P. Dahl, G. Lindström, K. Wiberg and C. Rappe, Chemosphere, 1995, 30, 2297.

51
M. S. McLachlan

plays a significant role for the higher chlorinated congeners. Although dry
gaseous deposition is a partitioning process, a partitioning equilibrium is not
approached. The uptake is limited by the rate of transport of chemical to the plant
surface, and thus the accumulation of PCDD/Fs in plants is primarily a function
of the gaseous concentration, the turbulence in the atmosphere and the length of
exposure. PCDD/Fs in plants are ingested by livestock. The absorption of the
different congeners is variable, decreasing from relatively high values of 30—80%
for the Cl —Cl DD/F to at most several percent for the Cl DD/Fs. Once in the
4 5 8
animal, most of the 2,3,7,8-substituted congeners are persistent and either
accumulate in fatty tissue or, in the case of cows and hens, are excreted in milk and
eggs. From there they are ingested by humans. Little is known about the degree of
absorption in adults, but PCDD/Fs accumulate to much higher levels in humans
than in livestock. This contaminant is transferred to nursing infants through the
mothers’ milk, and here it has been shown that the ingested PCDD/Fs are
virtually completely absorbed. Consequently, nursing infants are subject to the
highest daily dose on a body weight basis.
The biological uptake and transfer of PCDD/Fs in agricultural food chains has
also been examined from a bioaccumulation perspective using fugacities.79 In
aquatic food chains, persistent lipophilic organic contaminants are often
biomagnified, which means that their fugacity or lipid-based concentration
increases as the contaminant moves up the food chain. However, in agricultural
food chains there is a biodilution of PCDD/Fs, with the fugacity decreasing by up
to three orders of magnitude between air and cows’ milk. This can be attributed to
the kinetically limited uptake in plants, which prevents the achievement of an
air/plant partitioning equilibrium, and to the reduced absorption of the more
lipophilic congeners in livestock. This biodilution phenomenon is fortuitous,
since if food products were in equilibrium with the air then human exposure to
PCDD/Fs would be much higher.
It is important to note that the degree of accumulation of PCDD/Fs in
agricultural food chains differs from congener to congener. This is due primarily to
the behaviour in livestock, where many congeners are metabolized and others are
preferentiallytransferred to food products owing to more efficient absorptionfrom
feed. Consequently, two PCDD/F sources with similar toxicity equivalents might
pose very different risks to the food supply and human exposure. For instance, a
source contributing primarily 1,2,3,7,8-Cl DF would be of much less concern than
5
a source contributing 2,3,4,7,8-Cl DF, since most of the former compound would
5
be metabolized in livestock. Hence it is not possible to compare the risk from
different sources or contaminated environmental matrices on the basis of the
TEQs. This must be done on a congener by congener basis or using exposure
toxicity equivalents, a modification of the TEQ system that accounts for the
differences in the uptake and transfer behaviourbetween the PCDD/F congeners.89

8 Acknowledgements
The author thanks Kerstin Welsch-Pausch for preparing Figure 1.

89 M. S. McLachlan, Chemosphere, 1993, 27, 483.

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