Dairy ruminant exposure to persistent organic

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S 8 PAHs. Urban area (NL). Bakker et al. (2000). Rychen, Jurjanz, Toussaint and ...... Helling CS, Isensee AR, Woolson EA, Ensor PJD, Jones GE, Plimmer JR and .... Olling M, Derks HJGM, Berende PLM, Liem AKD and de Jong APJM 1991.
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Animal (2008), 2:2, pp 312–323 & The Animal Consortium 2008 doi: 10.1017/S1751731107001139

Dairy ruminant exposure to persistent organic pollutants and excretion to milk G. Rychen-, S. Jurjanz, H. Toussaint and C. Feidt Nancy University, UR AFPA, INRA, 2 avenue de la Foreˆt de Haye, 54505 Vandoeuvre cedex, France

(Received 30 April 2007; Accepted 25 September 2007)

Human activities produce polluting compounds such as persistent organic pollutants (POPs), which may interact with agriculture. These molecules have raised concern about the risk of transfer through the food chain via the animal product. POPs are characterised by a strong persistence in the environment, a high volatility and a lipophilicity, which lead to their accumulation in fat tissues. These compounds are listed in international conventions to organise the information about their potential toxicity for humans and the environment. The aim of this paper is to synthesise current information on dairy ruminant exposure to POPs and the risk of their transfer to milk. Three major groups of POPs have been considered: the polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), the polychlorobiphenyls (PCBs) and the polycyclic aromatic hydrocarbons (PAHs). The results show that contamination of fodder and soil by these compounds is observed when they are exposed to emission sources (steelworks, cementworks, waste incinerators or motorways) compared with remote areas. In general, soil contamination is considered higher than plant contamination. Highest concentrations of POPs in soil may be close to 1000 ng/kg dry matter (DM) for PCDD/Fs, to 10 000 mg/kg DM for PAHs and 100 mg/kg DM for PCBs. The contamination of milk by POPs depends on environmental factors, factors related to the rearing system (fodder and potentially contaminated soil, stage of lactation, medical state of the herd) and of the characteristics of the contaminants. Transfer rates to milk have been established: for PCBs the rate of transfer varies from 5% to 90%, for PCDD/Fs from 1% to 40% and for PAHs from 0.5% to 8%. The differential transfer of the compounds towards milk is related to the hydrophobicity of the pollutants as well as to the metabolic susceptibility of the compounds. Keywords: milk, plants, pollutants, ruminant, soil

Introduction Human activities produce polluting compounds such as persistent organic pollutants (POPs), which may impair agriculture and consequently food safety (Antignac et al., 2006). These compounds have raised concern about the risk of transfer through the food chain and particularly via milk (Rychen et al., 2005 and 2006). POPs are considered as persistent compounds in the environment. Particular attention has been given to compounds characterised by involuntary emission through incomplete combustion: polychlorodibenzo-p-dioxins (PCDDs), polychlorodibenzofurans (PCDFs), polychlorobiphenyls (PCBs) or non-chlorinated compounds such as polycyclic aromatic hydrocarbons (PAHs). These hydrophobic compounds are known to be persistent in the environment depending on the chlorination and the number of aromatic cycles (Laurent et al., 2005). -

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Atmospheric deposition is usually the primary vector of lipophilic contaminants into plants (Welsch-Pausch et al., 1995; Thomas et al., 1998). Several authors have detected an increase of POP concentrations in milk produced near potential POP emission sources (Rappe et al., 1987; Stevens and Gerbec, 1988; Eitzer, 1995; Hippelein et al., 1996; Ramos et al., 1997; Grova et al., 2002a; Tieyu et al., 2005) such as steelworks, cementworks, waste incinerators or motorways. POP contamination has been described in different environmental matrices such as plants or soil (Bryselbout et al., 2000). Thus, lactating ruminants may be exposed to POPs when polluted roughage or soil is ingested during grazing. Indeed, cattle can ingest up to 1.5 kg soil (Fries, 1996) per day depending on the climatic zone, season and grass density (Healy, 1968; Mayland et al., 1975). The aim of this paper is to present an overview of the current knowledge on dairy ruminant exposure to POP via plants and soil and their transfer to milk.

Dairy ruminant exposure to persistent organic pollutants Exposure of dairy ruminants to POPs via plants or soil

Contamination of plants After being emitted, POPs are directed towards the earth’s surface in the form of gas or particulate deposits according to environmental conditions (Pavlı´kova´ et al., 2007). The atmospheric transport of these compounds may be responsible for the contamination of sites quite distant from any source of emissions (Lohman and Seigneur, 2001; Garban et al., 2002). Several authors (Bennett et al., 1998, Van Pul et al., 1998; Beyer et al., 2000) have stated that some PCDD compounds tetrachlorodibenzo-p-dioxin (TCDD) and octachlorodibenzo-p-dioxin (OCDD) may be distributed over hundreds of kilometres. This phenomenon has also been observed for PCBs (Teil et al., 2004). Thus, Thomas et al. (1998) did not find any differences in PCB grass contamination between a rural area and in grass collected in an industrial area. The levels and profiles of PAHs and platinum group elements (PGE except Rh) in highway grasses transferred to a remote area did not significantly decrease, suggesting a potential risk of contamination for dairy ruminants (Tankari Dan-Badjo et al., 2007). For PAHs, some compounds can also be transported over long distances (Menichini et al., 2007); however, the heaviest PAHs are generally deposited near the emission site (Koeleman et al., 1999). Cre´pineau et al. (2003) showed, for example, that grass samples collected in a rural area may be significantly less contaminated than samples collected in the vicinity of motorways. Tables 1 and 2

indicate grass contamination levels by polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), PCBs or PAHs and reveal different levels depending on environmental conditions such as emission sources or climate parameters. Highest concentrations are generally found in the vicinity of a hazardous waste incinerator (PCDD/Fs or PCBs) or in the vicinity of motorways (PAHs) (Lee et al., 2004 and 2005).

Mode of contamination of plants. The plant being the interface between the soil and the atmosphere, its contamination is likely to occur either by atmospheric deposit or by root absorption (Yang and Zhu, 2007). Four ways of entry of POPs have been distinguished (Welsch-Pausch et al., 1995; Bakker et al., 2000 and 2001; Teil et al., 2004): gas deposit, the dry deposit of particles, the wet deposit of particles and root absorption. Each mode of contamination must be taken into account in order to evaluate the entry of the pollutants into the plant, their availability for the ruminant, and to characterise and model the contamination of fodder. Contamination by root absorption is considered by many authors as negligible (Wild et al., 1992; WelschPausch et al., 1995; Kipopoulou et al., 1999; Ouvrard et al., 2006) since the POPs are not very soluble in water but are very lipophilic compounds (Simonich and Hites, 1994). Gas deposit concerns the most-volatile compounds, namely the least-chlorinated PCBs and the low-molecular-weight PAHs with two or three aromatic cycles (Howsam et al., 2000).

Table 1 Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and polychlorobiphenyls (PCBs) levels in grass samples collected near a cimentory (CIMEN), a hazardous waste incinerator (HWI) or a rural area (control)

Compounds-

Welsch-Pausch and MacLachlan (1998)

Schuhmacher et al. (2004)

Costera et al. (2006)

PCBs

Costera et al. (2006)

Costera et al. (2006)

Control (ng/kg)

CIMEN (ng/kg)

HWI (ng/kg)

Compounds

Control (ng/kg)

HWI (ng/kg)

0.07 0.07 0.09 0.27 0.19 3.07 24 0.89 0.24 0.28 0.21 0.09 0.04 0.08 1.20 0.10 1.3

nd0.04 0.08 0.10 0.06 0.62 1.68 0.21 0.11 0.11 0.11 0.10 nd 0.10 0.39 0.06 0.43

0.06 0.65 0.64 0.68 0.61 4.65 10.33 0.35 0.62 1.00 1.18 1.37 0.20 1.73 4.69 0.35 1.49

3.86 0.14 0.63 0.12 19.45 1.27 63.69 2.23 6.68 1.17 4.57 0.9 57 46 169 176 319 68

10.43 0.59 3.02 1.03 42.42 2.49 126.7 5 13.82 2.87 8.26 2.22 66.76 68.53 215.57 283.42 457.98 126.45

2,3,7,8-TCDD 1,2,3,7,8-PeCDD 1,2,3,4,7,8-HxCDD 1,2,3,6,7,8-HxCDD 1,2,3,7,8,9-HxCDD 1,2,3,4,6,7,8-HpCDD OCDD 2,3,7,8-TCDF 1,2,3,7,8-PeCDF 2,3,4,7,8-PeCDF 1,2,3,4,7,8-HxCDF 1,2,3,6,7,8-HxCDF 1,2,3,7,8,9-HxCDF 2,3,4,6,7,8-HxCDF 1,2,3,4,6,7,8-HpCDF 1,2,3,4,7,8,9-HpCDF OCDF

-

PCDD/Fs

PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB PCB

77 81 126 169 105 114 118 123 156 157 167 189 28 52 101 138 153 180

TCDD 5 tetrachlorodibenzo-p-dioxin; PeCDD 5 pentachlorodibenzo-p-dioxin; HxCDD 5 hexachlorodibenzo-p-dioxin; HpCDD 5 heptachlorodibenzo-p-dioxin; OCDD 5 octachlorodibenzo-p-dioxin; TCDF 5 tetrachlorodibenzofuran; PeCDF 5 pentachlorodibenzofuran; HxCDF 5 hexachlorodibenzofuran; HpCDF 5 heptachlorodibenzofuran; OCDF 5 octachlorodibenzofuran; -nd: not detected. -

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Rychen, Jurjanz, Toussaint and Feidt Table 2 Mean polycyclic aromatic hydrocarbons (PAHs) levels in grass samples collected in different areas (ng/g)

Compounds

Sampling sites

142 1461 100 to 900 136 to 510 153 900 25 200 to 1 700

S 16 PAHs S 16 PAHs S 24 PAHs

Road (13 000 cars per day) Highway (F) Rural area (UK) Rural area (UK) Urban area (UK) Highway (F) Rural pasture Urban area (NL)

S 16 PAHs S 16 PAHs S 16 PAHs S 8 PAHs

The least-volatile compounds are found mainly in the form of particulate deposit (Welsch-Pausch et al., 1995). Thus, PCDD/Fs are found deposited in the particulate form, PCBs are found primarily in the gas form (Thomas et al., 1998) and the PAHs are found in one form or the other, or in both forms according to their octanol–air partition coefficient (KOA). Generally, the concentration in the plants depends on the distribution and nature of the compounds in the atmosphere and their properties influencing the proportion between the particulate and the gas form.

Factors influencing POP deposit. Environmental conditions, characteristics of the plants and physicochemical properties of the compounds represent numerous factors that may influence the type of deposit and the quantity of pollutants found on the plant (Oleszczuk and Baran, 2005). The main environmental conditions influencing the content of POPs in plants are temperature, rainfall and wind. Temperature affects the form in which the POP compounds are present in the atmosphere: gas or particulate (Howsam et al., 2000; Bakker et al., 2001; Blais et al., 2003). Some compounds are thus present in the atmosphere in particulate or gas form according to the ambient temperature (KOA of the compounds is temperature dependent): this is the case, for example, of the TCDD, which is exclusively in gas form during the summer (Welsch-Pausch and MacLachlan, 1998). The concentration of the pollutants in vegetation also depends on temperature: it increases by a factor of 30 to 2000 when the temperature increases from 58C to 508C (Bakker et al., 2001). Wind speed and direction also affect the concentration of POPs in plants (Bakker et al., 2001; Lohman and Seigneur, 2001; Smith et al., 2001; Teil et al., 2004) by modifying the distribution of the compounds in the atmosphere. The role of rainfalls on the rinsing of the compounds depends on their nature and the plant concerned: for example, a lettuce washed with water involves a significant extraction of high-molecular-weight PAHs; however, water will extract only a weak part of high molecular PAHs or PCDD/Fs in corn (Bakker et al., 2001). POP concentrations in plants are also dependent on the characteristics of the plant such as the pilosity of the sheet, the composition of the cuticle or the architecture of the plant. The cuticle, rich in waxes, can involve an increase in 314

References Mu¨ller et al. (2001) Bryselbout et al. (2000) Smith et al. (2001) Meharg et al. (1998) Cre´pineau et al. (2003) Cre´pineau-Ducoulombier and Rychen (2003) Bakker et al. (2000)

the accumulation of the lipophilic molecules (Mu¨ller et al., 2001). Cutin, composing the cuticle, is responsible for 70% to 90% of adsorption (Thomas et al., 1998) and it is the quality of waxes present rather than the thickness of the cuticle that modifies the concentration (Smith et al., 2001). There is a passive diffusion between the atmosphere and the cuticle in the case of gas deposits. The molecules are transferred until an air–plant balance is reached. The time to reach balance varies according to species: from 24 to 240 s for the citrus kind and from 58 to 580 days for the Ilex kind (Bakker et al., 2001). Thus for certain plants, a balance is never reached because the lifespan of the plant is too short (Thomas et al., 1998; Smith et al., 2001). Furthermore, the surface of deposit of the plants is also a major factor affecting POP deposit: it is, for example, 6 to 14 times higher than that of the soil on which they develop (Simonich and Hites, 1994). The physicochemical characteristics of the various POPs are also among the principal factors influencing the contamination of grass. The proportion of the gas or particulate phase depends on the characteristics of the molecules (Howsam et al., 2000) and, in particular, of their volatility (Bakker et al., 2001), their lipophilicity measured by the KOA value (coefficient of distribution octanol–air), their solubility in water, their steam pressure value, their constant of Henry (Meneses et al., 2002) and their half-life (Kipopoulou et al., 1999). The value of KOA varies according to the compounds and directly influences the distribution of gas particles (Lohmann and Jones, 1998). When the KOA is high, the particulate deposit increases. For example, PCBs with high chlorination have a low steam pressure and high KOA and thus are found in the particulate form (Jan et al., 1994). The PCDD/Fs having six chlorine atoms or more are also in the particulate form (Bakker et al., 2001). The PAHs with two and three cycles are exclusively in the gas form and those with more than five cycles are mainly in the particulate form. The PAHs with four cycles are distributed between the two forms according to the ambient temperature (Howsam et al., 2000). This great variability is important for a better understanding of the profiles detected in the plants. For example, 95% of phenanthrene is always in the gas form whereas this value is less than 10% for benzo[g,h,i] perylene (Wild et al., 1992).

Dairy ruminant exposure to persistent organic pollutants

Contamination of soil Soil contamination by organic pollutants occurs primarily by atmospheric deposit (Laurent et al., 2005). When deposited on the surface of the soil, these compounds tend to remain in the superficial surface (the first 15 cm of soil) (Fries, 1982; Stevens and Gerbec, 1988; Jones et al., 1989). The sources of pollution of the soil correspond to three groups according to Wild and Jones (1995) and Lichtfouse et al. (1994 and 1997): industrial activities (energy production, metallurgy, chemical industries, etc.), urban activities (the transport, management and processing of waste) and husbandries (mud spreading) (Tables 3 and 4). Highest concentrations of POPs in soil may be close to 1000 ng/kg dry matter (DM) for PCDD/Fs (Table 3), to 10 000 mg/kg DM for PAHs (Table 4) and 100 mg/kg for PCBs (Krauss and Wilcke, 2003). Many authors have highlighted the fact that the concentration of organic pollutants in the soil increases with the increasing density of the human activities. The industrial activities that are most polluting in PAHs and chlorinated compounds are those using fossil fuels (Edwards, 1983; Kakareka, 2002; Krauss and Wilcke, 2003). Another source of contamination of the soil is the production of coke from coal. Indeed, the mechanisms of condensation, decantation and distillation of the tar from the furnace (tar being a by-product of the manufacture of coke) generate the formation of organic pollutants, which are then emitted into the atmosphere. In addition, soil contamination by PAHs, PCDD/Fs and PCBs is often concomitant with those of metal pollutants. It is known that lignite combustion generates large quantities of PAHs and certain metals (chromium and nickel). In the same way, the PCDD/Fs, the PCBs and 12 trace elements (Ag, Cd, Co, Cr, Cu, Mn, Ni, Pb, Sn, Tl, V, Zn) are released in the atmosphere

bordering the sites of cementworks. Henner (2000) also points out that another source of soil pollution by PAHs is the sites of gas extraction. These direct contaminations of soil by atmospheric emissions, of anthropogenic origin, may be increased by indirect effects such as the degeneration of the plants. Indeed, 44 6 18% of the atmospheric PAHs are introduced into the soil following their capture on waxy surfaces of plants followed by the decomposition of the plant (Simonich and Hites, 1994). The pollution of soil can also result from the natural contribution of organic pollutants (for example, the pyrolysis of humus during forest fires) (Laurent et al., 2005). Because of their lipophilic character and a low aqueous solubility, there is a strong POP adsorption in the organic matter of the soil. The rinsing of the soil POPs is thus regarded as negligible (US EPA, 2000).

Availability of POPs in soil. The availability of pollutants in soil depends on their physicochemical properties (solubility, steam pressure, Kow (octanol–water coefficient), constant of Henry), environmental factors (temperature, precipitations, dissemination of the contaminated particles) and other specific factors such as the type of culture in relation to the characteristics of the root system (Duarte-Davidson and Jones, 1996). However, the main factor results from the characteristics of the soil (composition and contents of organic matter and humic acid, pH and potential of oxydoreduction) (White et al., 1997; Robertson and Alexander, 1998; Moon et al., 2003). These parameters control the rates of absorption/desorption of the pollutants of the soil and thus the distribution of these substances in the three phases (liquid, gas and solid) of this matrix (Billeret et al., 2000; Chiou et al., 2000; Huang et al., 2003). For PAHs,

Table 3 Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) levels in various soil samples collected near a waste incinerator (WI), a cimentery (CIMEN) or in rural area (control)-

Compounds 2,3,7,8-TCDD 1,2,3,7,8-PeCDD 1,2,3,4,7,8-HxCDD 1,2,3,6,7,8-HxCDD 1,2,3,7,8,9-HxCDD 1,2,3,4,6,7,8-HpCDD OCDD 2,3,7,8-TCDF 1,2,3,7,8-PeCDF 2,3,4,7,8-PeCDF 1,2,3,4,7,8-HxCDF 1,2,3,6,7,8-HxCDF 1,2,3,7,8,9-HxCDF 2,3,4,6,7,8-HxCDF 1,2,3,4,6,7,8-HpCDF 1,2,3,4,7,8,9-HpCDF OCDF

Lorber et al. (1994)

Schuhmacher et al. (2004)

Domingo et al. (2002)

Blanchard (2001)

Control (ng/kg)

CIMEN (ng/kg)

WI (ng/kg)

WI (ng/kg)

0.88 nd nd 4 9 194 237 1.59 nd nd nd nd nd 2 47 nd 30.2

nd0.09 0.12 0.2 0.2 3.7 25.3 0.25 0.15 0.17 0.18 0.2 0.04 0.22 1.05 0.08 0.37

0.41 1.31 1.48 4.03 4.23 46.93 761.36 12.74 2.23 4.73 10.55 3.27 0.23 4.47 21.20 2.44 21.54

0.11 0.45 0.52 1.25 0.8 15.38 75.04 1.32 0.45 1.27 1.82 1.63 0.53 2.02 8.03 1.33 11.77

-

See foonote of Table 1 for abbreviations.

315

Rychen, Jurjanz, Toussaint and Feidt Table 4 Polycyclic aromatic hydrocarbons (PAH) levels in various soil samples collected near a highway (HIWA), a coke manufacture (COMA), a gas manufacture (GAMA), a petrochemic industry (PEIN) or in an urban area (URAR) or a forest (FORE)-

Naphtalene Acenaphtene Ace´naphtylene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[a]anthracene Chrysene Benzo[b]fluo-ranthene Benzo[k]fluo-ranthene Benzo[a]pyrene Indenol[1,2,3-cd]pyrene Benzo[g,h,i]perylene Dibenzo[a,h]anthracene

Cre´pineau et al. (2003)

Wild and Jones (1995)

HIWA (mg/kg DM)

URAR (mg/kg DM)

15 4 12 5 76 13 162 123 79 126 163 54 70 93 102 48

6 37 nd nd 14 2 27 31 20

154 86 nd nd 533 117 1132 573 796

nd227 nd nd 379 156 2174 4911 662

10 nd 7 nd 33 nd

492 nd 352 nd 685 nd

92 nd 260 nd nd nd

Wild and Jones (1995)

Wild and Jones (1995)

Juhasz and Naidu (2000)

Juhasz and Naidu (2000)

FORE (mg/kg DM) COMA (mg/kg DM) GAMA (mg/kg DM) PEIN (mg/kg DM) nd 2 nd 225 379 1156 2174 91 317 345 2271 92 120 nd 192

1131 nd 333 650 1595 334 682 642 nd 614 nd nd nd nd nd nd

-

nd 5 not determined.

Wild et al. (1990) showed that time of half-life lies between 2 months and 9 years, respectively, for naphthalene and benzo[g,h,i]perylene. For the chlorinated compounds, times of half-life in the soil fluctuate between 6 months (example of the PCB ‘dioxins-like’) (Cousins and Jones, 1998) and tens of years (example of the OCDD) according to the degree of chlorination of the compounds (Laurent et al., 2005).

Abiotic and biotic degradation of bound soil organic pollutants. The degradation of POPs in soil can be carried out by photodegradation and microbial degradation (Laurent et al., 2005). These phenomena generate the appearance of metabolites, with a change in the chemical structure, and cause modifications of their toxicity (in particular, for the PAH) and of their behaviour in the soil compared with that of the parent compounds (Schiavon, 1988). The photodegradation or abiotic degradation of the organic pollutants can take place only for the compounds located at the soil surface (Hebert and Miller, 1990). PAHs can be degraded by photo-oxidation and reactions of oxidation (Juhasz and Naidu, 2000). They react with ozone to form quinones and epoxides. This mechanism is relatively important and allows a clear reduction in soil PAHs. The mechanism of photodegradation of the PCDD/Fs and the PCBs ‘dioxins-like’ has been the subject of some studies (Moore and Ramworthy, 1984; Dougherty et al., 1993; McPeters and Overcash, 1993). It implies a dechlorination (Helling et al., 1973), the slightly chlorinated molecules being more easily photolysed than the octa-chlorinated compounds (Helling et al., 1973; Dougherty et al., 1993). However, this mechanism would not be very important since soil limits the penetration of ultraviolet radiation. However, Miller et al. (1989), 316

Kieaitwong et al. (1990) and Tysklind et al. (1992) highlighted that the chlorine atoms, in a peri position (1,2,5,6), from the strongly chlorinated PCDD were eliminated, thus leading generally to the formation of the 2,3,7,8-TCDD. The microbial or biotic degradation of the organic pollutants of the soil is a mechanism controlled by the temperature, by the properties of the soil (water and organic matter content, pH) and the compounds (molecular weight and log Kow) (Cerniglia, 1992; Bakker and Vries, 1996; Mhiri and Tandeau de Marsac, 1997). These activities of POP degradation in the soil play a role in the carbon cycle. PAHs are composed of carbon and hydrogen and thus form an integral part of this cycle (Gibson and Subramanian, 1984). Indeed, their similarity with other organic molecules means that telluric microorganisms have the enzymatic ability to degrade them. Thus, microbial degradation is a more important process of decontamination of soils than the process based on the photo-oxidation or self-oxidation. In a general way, the mechanism is accelerated in the presence of nutrients added (oil) to the soil (Wilson and Jones, 1993; Straube et al., 1999), of organic matter (Ka¨stner and Mahro, 1996), of a ventilation of the soil and an increase in temperature (Bonten et al., 1999), these different factors probably supporting the development of microorganisms. Microbial degradation of PCBs is carried out accordingly in one of two ways: the strongly chlorinated compounds can undergo a dechlorination in anaerobic conditions while the others generally undergo an oxidation by bacteria developing in aerobiosis (Abramowicz, 1990). The importance of this microbial degradation is still being discussed (Pizzul et al., 2007). According to Mhiri and Tandeau de Marsac (1997), the biological breakdown of soil PCBs

Dairy ruminant exposure to persistent organic pollutants allows a significant elimination of these molecules, whereas for Sierra et al. (2003), these same molecules are slightly metabolised. It is the same for the PCDD/Fs: in a general way, the degradation of the PCDD/Fs by bacteria of the soil is regarded as a rather ineffective way of dissipation, requiring many years and particularly when the compounds are strongly chlorinated (Arthur and Frea, 1989; Parsons and Storms, 1989; Paustenbach et al., 1992; Aust and Benson, 1993; Beurskens et al., 1995; Ballerstedt et al., 1997; Wittich, 1998). Habe et al. (2001 and 2002) highlighted that after 7 days of inoculation with Terrabactersp. (stock DBF63) the rate of degradation of the molecules with four to six chlorine atoms was close to 10%, whereas for the highest-chlorinated compounds it was close to zero. Transfer of POPs to milk The different ways of contamination of the dairy ruminant by POP are ingestion of polluted feed or soil, inhalation of contaminated air or absorption by dermal contact. In the lactating animal, the exposure by inhalation is considered as negligible when compared with the oral administration of contaminated feed or soil. The skin absorption of organic pollutants present in the soil or the plants was not studied, but several studies undertaken on laboratory animals suggest that this exposure is also negligible under the conventional conditions of breeding. Therefore, research work has been focused towards the contamination of the ruminant via the feed, i.e. the ingestion of roughage or soil. Indeed, a lactating ruminant may ingest daily from 1% to 10% soil when grazing (Healy, 1968; Thornton and Abrahams, 1983). The contamination of milk by POPs depends on environmental factors, factors related to the rearing system (fodder and potentially contaminated soil, stage of lactation, medical state of the herd) and to the characteristics of the contaminants.

Factors influencing POP transfer to milk Several authors measured the concentrations of PCDD/Fs in milk produced in farms located either near or far from polluting sources (Rappe et al., 1987; Schmid and Schlatter, 1992; Eitzer, 1995; Harrison et al., 1996; Hippelein et al., 1996; Ramos et al., 1997; Schulz et al., 2005). In milks produced in isolated farms far from POP emission sources, the contents of PCDD/Fs were found to be between 1.3 and 2.5 pg I-TEQ/g of fat content. In the POP-exposed situations, the concentrations in PCDD/Fs were also generally lower than the threshold of 3 pg I-TEQ/g of fat content. However, in some extreme situations, values reaching 9 pg I-TEQ/g of fat content have been found (Costera et al., 2006). An increase in the contents of 2,3,4,7,8-pentachlorodibenzofuran (PeCDF), 1,2,3,4,7,8-HxCDD/F, 1,2,3,6,7,8-HxCDD/ F, 2,3,4,6,7,8-hexachlorodibenzofuran (HxCDF) and 2,3,7, 8-TCDD is noted around chemical, metallurgical industries or waste incinerators. For PCDD, the concentrations of compounds in milk appeared to be linked to the number of

chlorine atoms carried by the molecule (Ramos et al., 1997). The PCDD/F contents of milk are also dependent on rearing factors. Indeed, POP transfer to milk may fluctuate according to the physiological status of the animals. Tuinstra et al. (1992) showed, for example, that the disappearance of the PCDD/Fs in milk was linked to the body fat reserves of the animal. The mobilisation of these reserves during the cycle of lactation can thus have a significant impact on the content of PCDD/Fs in milk. Indeed, at the beginning of lactation, lactating animals do not manage to meet their needs via feed intake and therefore use their body fat reserves. Later during lactation, the opposite phenomenon (nutritive contribution in excess compared with the needs) occurs and POPs may be stored in body fat reserves (Jarrige, 1988; Thomas et al., 1999). Thus, the peak of concentration of PCDD/Fs observed in the colostrum (Tuinstra et al., 1992) could be related to the contamination of the animal during its phase of reconstitution of the body reserves during the previous lactation. The medical status of the lactating ruminant also modulates the contents of PCDD/Fs in milk. Indeed, Fries et al. (1999) noted an increase in the concentrations of PCDD/Fs strongly chlorinated during the infection of the mammary gland. This phenomenon can be explained by the structural modifications of the cells of the mammary gland at the time of a mastitis (with an increase in the permeability of the mammary epithelial barriers) (Fries et al., 1999). Mammary epithelium could play a key role in the selective transfer of PAH from food to milk (Cavret et al., 2005). Milk levels of POPs can also fluctuate during lactation according to seasons and according to the diets of the animals (Krokos et al., 1996). Indeed, during the summer period (animals in pastures), the involuntary ingestion of soil whose POP contamination is generally higher than that of grass can represent a major concern (Fries and Paustenbauch, 1990). Mamontova et al. (2007) found, for example, a good correlation between PCB levels in autumn milk and in soil. These authors suggested that ingestion of pasture soil was the dominant source of PCBs in milk. However, these limited data suggest the need for further investigations.

Transfer rates of POPs to milk When considering the transfer of POP to milk, the PAHs and the chlorinated compounds need to be distinguished: PCDD/ Fs and PCBs are generally considered as persistent and bioaccumulable in the livestock products whereas PAH are considered as largely metabolised. Although the physicochemical characteristics of these compounds are well described, their interaction with the metabolism of the dairy ruminant is not yet well known. Transfer of PCDD/Fs and PCBs to milk. Table 5 indicates the values of the PCDD/Fs transfer rates ‘feed–milk’ determined by several authors. The obtained values oscillate between 1% and 52.8% according to the compounds and it is 317

Rychen, Jurjanz, Toussaint and Feidt and Jones, 1996; Focant et al., 2003). In a recent study (Mamontova et al., 2007), the relationship between PCB levels in cow’s milk and in pasture soil was assessed and proved. In another recent study (Costera et al., 2006), the feed to milk transfer of 17 PCDD/Fs and 18 PCBs was established in lactating goats exposed to a 10-week intake of contaminated hay collected in the vicinity of a hazardous municipal waste incinerator. For PCDD/Fs (Table 5), 2,3,7, 8-TCDD appeared as the compound having the highest carry-over rate (52.8%). For dioxin-like PCB, carry-over rates higher than 80% were obtained for PCBs 105, 118 and 157. Concerning indicators PCB, the carry-over rates ranged from 5% (PCB 101) to more than 40% (PCBs 118, 153 and 180) (Figure 1). According to Costera et al. (2006), the intensity of the transfers appeared as a function of both the physicochemical properties (chlorination or log Kow) of the compounds and their metabolic behaviour. This observation indicates a marked biotransformation of the different compounds by the ruminant (Firestone et al., 1979; Rappe et al., 1987; Olling et al., 1991; Fries et al., 1999; McLachlan, 1999). According to Willett et al. (1989), the PCBs may be partially degraded during the fermentation of the ration in the rumen. Results reported in Table 5 indicate similar carry-over rates of PCCD/Fs in lactating cows and lactating goats. These experimental carry-over rates obtained in different locations and feeding systems do argue for a similar behaviour of the chlorinated compounds in the two different animal species. Therefore, the lactating goat may be considered as a valuable ‘lactating animal model’ to investigate the POP transfer from feed to milk.

noticeable that all the individual PCDD/F compounds were found in milk. For the compounds whose log Kow is higher than 6.5, the transfer appeared to decrease with the increase of the log Kow value. Generally, transfer rates decreased with the number of chlorinations. Some exceptions however have been detected: among the PCDFs, the weak transfer of 2,3,7,8-tetrachlorodibenzofuran (TCDF), 1,2,3,7,8-PeCDF and 1,2,3,7,8,9-HxCDF may be related to the hepatic degradation of the compounds. The contents of PCBs in cow’s milk have been less studied: concentrations were usually in the range of 1 pg/g fat, except for PCB 118 whose concentrations reached levels 1000 times higher (Willett et al., 1987 and 1989; Krokos et al., 1996; Sewart Table 5 ‘Feed–milk’ transfer rates of polychlorinated dibenzo-p-dioxins and dibenzofuransFries et al. (1999)

Costera et al. (2006)

Lactating cows

Lactating goats

35 28 18 16 12 1.8 0.3 nd nd 18 5.7 11 nd 8.4 1.4 nd 0.1

52.8 33.1 23.7 25.0 15.0 5.4 1.7 10.2 14.3 29.4 21.8 18.0 3.0 12.5 2.7 3.5 0.9

Compounds 2,3,7,8-TCDD 1,2,3,7,8-PeCDD 1,2,3,4,7,8-HxCDD 1,2,3,6,7,8-HxCDD 1,2,3,7,8,9-HxCDD 1,2,3,4,6,7,8-HpCDD OCDD 2,3,7,8-TCDF 1,2,3,7,8-PeCDF 2,3,4,7,8-PeCDF 1,2,3,4,7,8-HxCDF 1,2,3,6,7,8-HxCDF 1,2,3,7,8,9-HxCDF 2,3,4,6,7,8-HxCDF 1,2,3,4,6,7,8-HpCDF 1,2,3,4,7,8,9-HpCDF OCDF

PAH transfer to milk. Studies on PAH transfer in the terrestrial food chain appear limited owing to the fact that these compounds are known to be strongly metabolised. These molecules have nevertheless a recognised toxicity. PAH

-

See foonote of Table 1 for abbreviations; nd 5 not determined.

120.0

a 100.0

ab

b

ab b

bc

COR (%)

80.0

d

cd

60.0

d

cd

d

d e

40.0

ef efg

fg

20.0

fg g

a-g

0

3

18

8

B PC

B PC

Va lues without common letters are significantly different (P0.05)

Figure 2 Polycyclic aromatic hydrocarbons (PAHs) and hydroxy polycyclic aromatic hydrocarbons (OH-PAHs) excretion in milk and urine (0 to 24 h) after a single oral administration of the compounds (Lapole et al., 2007). a,bMean values with similar letters do not differ significantly (P . 0.05).

increase in higher amounts. These metabolites are much less hydrophobic than the native molecules and can therefore be excreted through urine. Conclusion Data presented in this review indicate that POPs present in roughage or in soil are transferable towards livestock products and milk in particular. Knowledge of the levels of pollutants in roughage or soil highlights the potential presence of the pollutants in various agricultural types of mediums. Therefore, there is a real need to better evaluate the location of the contaminated area in order to reduce ruminant exposure. At the very least, rearing practices that lead to soil ingestion should be avoided. Further research work should be carried out in order to define threshold values that should not be exceeded either in feed matrices or in soil. The animals are likely to intake varying quantities of POPs during grazing. In particular, the ruminant can involuntarily ingest soil whose level of contamination is generally higher than that of fodder. The analysis of the mechanisms of absorption, biotransformation and transfer also needs further research work. Scientific approaches such as toxicocinetic studies should be envisaged in order to better characterize the processes of absorption and elimination of the molecules in the dairy ruminant. The analytical approaches also need to be improved (gas chromatography/high-resolution mass spectrometry (GC-HRMS) and/or GC-MS/MS) for a better detection and quantification of the parent compounds and their metabolites. In addition, as human activities are likely to produce new polluting compounds (for example, 320

polybrominated compounds) it would be necessary to evaluate the risks of transfer of the emerging compounds in the food chain. Thus, there are some major fields of investigation that represent important questions in terms of food safety.

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