The whole dairy goat sector is responsible for the safety of its food products and feeds. Goat feeds, including herbage, may be subjected to contamination from diverse sources, such as environmental pollution and activities of insects and microbes. Undesirable substances that can occur in feedstuffs include organic compounds such as plant toxins, mycotoxins, dioxins and polychlorinated biphenyls (PCBs), and inorganic compounds, such as heavy metals. The effects of undesirable substances in feedstuffs range from reduced intake to reproduc- tive dysfunction and increased incidence of diseases in animals. Moreover, in many cases they can be transferred to edible animal products such as milk.
Mycotoxins
Mycotoxins are low-molecular-weight secondary metabolites, produced by fila- mentous fungi, which affect human and animal health. Mould growth and mycotoxin contamination of feedstuffs can occur at all stages of the production cycle (cropping, harvest, transport and storage). Mycotoxins can be found in feed ingredients, such as maize, sorghum grain, barley, wheat, rice meal, cotton- seed meal, groundnuts and other legumes. Most of them are relatively stable, not destroyed and, sometimes concentrated, during feed processing. The possibility of transferring mycotoxins or their metabolites to milk represents a potential risk to dairy consumers.
Aflatoxins, which are included among the substances carcinogenic to humans by the International Agency for Research on Cancer of the World Health Organi- zation (WHO) (IARC, 2002), represent the family of mycotoxins of major concern in goat husbandry. The ingested aflatoxin B1 (AFB1) is biotransformed by hepatic microsomal cytochrome P450 into aflatoxin M1 (AFM1), which is then excreted in the milk of lactating animals. The occurrence of AFM1 in goat’s milk has been reported in several studies (Roussiet al., 2002; Oliveira and Ferraz, 2007; Virdis et al., 2008). The concentration of AFM1 in goat’s milk reached a steady-state con- dition within days from the start of AFB1 intake (Smithet al., 1994). The carry-over value of AFB1 from feed into AFM1 was about 0.40% for goats receiving 124.4µg of AFB1 daily for 2 weeks (Rao and Chopra, 2001). In ruminants, the addition of sequestering agents, which bind to AFB1, reduced its absorption by the gastroin- testinal tract and attenuated the transfer of AFM1 to milk (Diazet al., 2004). In lactating goats, the addition of aluminosilicate or activated charcoal to feeds dramatically decreased AFM1 concentration in milk (Table 1.9; Fig. 1.4). The AFM1 concentration in unprocessed milk was linearly related to AFM1 concentra- tions in curd and whey (Battaconeet al., 2005). In a study on the AFM1 distribu- tion in different protein fractions in goat’s milk and during the production of goat’s cheese, neither ultrafiltration nor acidic or enzymatic treatments influenced the interaction between the toxin and casein or whey proteins (Barbiroliet al., 2007).
Several studies have reported that small ruminants appear to be tolerant to mycotoxins such as fumonisins (Gurunget al., 1998), ochratoxin A (Blanket al., 2003), zearalenone and trichothecenes (Kiesslinget al., 1984).
Dioxins and polychlorinated biphenyls
‘Dioxins’ is a term referring to the categories of polychlorinated dibenzo- p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs). These sub- stances occur mainly as by-products of incomplete combustion and of certain Aflatoxin
Contamination
(ppb) Adsorbent
Addition (%)
AFM1 in milk (ppb)
Length of administration
(days) Reference
Mixa 100
100 100 200 200
HSCAS HSCAS HSCAS HSCAS HSCAS
0 1 2 0 4
0.481±0.17 0.244±0.01 0.099±0.02 1.619±0.23 0.187±0.02
6 Smith
et al.
(1994)
Aflatoxin B1, pure
100 100 100
SB AC
0 1 1
0.498±0.085 0.164±0.041 0.091±0.028
14 Rao and
Chopra (2001) HSCAS, hydrated sodium calcium aluminosilicate; SB, sodium bentonite; AC, activated charcoal.
a79, 16, 4 and 1% of aflatoxins B1, G1, B2 and G2, respectively.
Table 1.9. Effect of different adsorbents on transfer of aflatoxin B1, as aflatoxin M1 (AFM1), in goat’s milk. The data are expressed as mean±standard error.
0 0.2 0.4 0.6 0.8 1.0 1.2
2 4 6 10 12
Length of administration (days)
Aflatoxin M1 (ppb)
HSCAS, 2% HSCAS, 1% HSCAS, 0%
Fig. 1.4. Effect on aflatoxin M1 concentration in milk of goats fed diets containing aflatoxins at 100 ppb in which 0%, 1% or 2% of hydrated sodium calcium alumino- silicate (HSCAS) was added. (Data from Smithet al., 1994.)
chemical processes. The toxicity of individual dioxin and dibenzofuran com- pounds (or congeners) varies considerably. The PCDD and PCDF congeners that are likely to be of toxicological significance are those with Cl atoms at the 2, 3, 7 and 8 positions, of which the most toxic is 2,3,7,8-tetrachlorodibenzo- p-dioxin. PCBs are chlorinated hydrocarbons synthesized by direct chlorination of biphenyl. Because there are PCB congeners that show similar toxicological properties to dioxins, these compounds are often termed ‘dioxin-like PCBs’.
PCDDs, PCDFs and PCBs are hazardous organic compounds of great importance to animal agriculture, because these compounds are persistent and tend to bioconcentrate in the lipids of tissues and products. All dioxins enter the food chain through animals that are exposed to contaminated surroundings and feeds, and tend to concentrate mainly in body and milk fat. Among foods of ani- mal origin, dairy products have the highest level of contamination (Bocioet al., 2003). The application of sewage sludge to agricultural land is a potential way of transporting the lipophilic halogenated hydrocarbon contaminants in animal tis- sues and products. When soil and pasture are contaminated by polychlorinated compounds, grazing animals (e.g. goats) are the most exposed to them, espe- cially when pasture is the major component of the diet, since soil ingestion is an additional contaminant source. Animal uptake of soil and plant contaminants is related to: (i) rates of soil ingestion; (ii) feeding and management systems; and (iii) bioavailability of contaminant molecules and their kinetics in animals (Fries, 1996). Dairy goats treated with PCB 126 and PCB 153 at doses of 49 and 98 ng/kg body weight (BW) per day, respectively, showed milk concentrations of PCB 126 and PCB 153 of 0.24 ng/g and 507 ng/g (wet weight), respectively (Lycheet al., 2004). The different kinetic properties observed for these two con- geners may have been due to hepatic sequestration of PCB 126 and accumula- tion of PCB 153 in fat tissue and milk in goats. In sheep, Vrecl et al. (2005) showed that PCBs were transferred from blood to either milk or faeces by two different pathways. In particular, an enrichment of lipophilic precursors was observed in milk, because of its higher lipid content compared with faeces. These results suggest that in lactating animals the higher chlorinated, coplanar and met- abolically stable PCBs are preferentially excreted in milk. Recently, Costeraet al.
(2006) determined the transfer of 17 PCDDs and PCDFs and 18 PCBs from feed to milk in Alpine lactating goats (mean BW: 50±5 kg) fed 800 g of contami- nated hay daily (2 ng/kg DM for WHO-PCDD/PCDF-TEQ versus 0.38 ng/kg DM for WHO-dioxin-like PCBs-TEQ, where TEQ is a dioxin toxic equivalent, calcu- lated by looking at all toxic dioxins and furans and measuring them in terms of the most toxic form of dioxin, (2,3,7,8-tetrachlorodibenzo-p-dioxin)) for 10 weeks.
The concentrations of the various compounds in milk were similar, with an increasing phase until a plateau was reached. For PCDDs/ PCDFs the plateau was reached after at least 35 days of contaminated hay intake. For PCBs, the steady state was reached very quickly, the latest being 22 days after the begin- ning of the experiment. The concentration of PCDDs and PCDFs ranged from 0.16 to 3.83 ng/g milk fat, while that of PCBs ranged from 2 to 3524 ng/kg milk fat. The carry-over rates of PCDDs, PCDFs and PCBs appeared to be a function of their physical and chemical properties, such as the number of Cl atoms and the metabolism of these compounds.
Polycyclic aromatic hydrocarbons (PAHs) are a large group of organic pol- lutants with two or more fused aromatic rings. They are mainly by-products of pyrolytic processes of organic materials during human activities, such as com- bustion of natural gas, processing of coal and crude oil, and vehicle traffic. These organic pollutants are ubiquitous and can occur at a low level of contamination in water, air or soil.
Owing to their physical and chemical properties, PAHs move through hydrophobic compartments of the food chain. In lactating animals, after inges- tion of contaminated feeds (e.g. pasture and forage), pollutants can be trans- ferred to milk. The selectivity of the mammary epithelial barrier, which favours the passage of lipophilic, low-molecular-weight compounds, suggests that mam- mary epithelium could play a key role in the selective transfer of PAHs from food to milk (Cavretet al., 2005). Grovaaet al. (2006) reported a rapid transfer of phenanthrene, pyrene and benzo(a)pyrene (PAH compounds), administered in a single dose, from feed to blood of lactating goats, and similar plasma kinetics for the three compounds. Both phenanthrene and pyrene showed a low milk transfer (1.6 and 1.9%, respectively), while benzo(a)pyrene showed a very low milk transfer (0.2%). Chronic oral exposure of lactating goats to different PAHs also confirmed that their transfer through the organism and excretion in milk is affected by the selectivity of the intestinal or mammary epithelial barrier for PAHs in lactating goats or by their capacity to metabolize them (Grovaaet al., 2006).
Heavy metals
Anthropogenic processes such as the combustion of coal and mineral oil, smelt- ing, mining, alloy processing and the paint industry are the major sources of heavy metals to animals in the vicinity of industrial areas. Animals allowed to graze on or fed contaminated pastures or fodders are continually exposed to these pollutants, leading to various health hazards. Also, agricultural activity may result in elevated levels of metals in soils. In particular, use of sewage sludge and long-term addition of inorganic fertilizers and pesticides can increase total and available metal contents in the upper soil horizons. Heavy metal accumulation in agricultural crops is particularly important in goat farming, because they are a source of toxic elements to the human food chain. Uptake and accumulation by crop plants represent the main entry pathway for potentially health-threatening toxic metals into human and animal food. In many cases, the relationship between metal content in the soil and in the crop is positive and linear (Grytsyuk et al., 2006).
For Cd, which is one of the most dangerous metals for animal and human health, the passage through the dairy food chain is not limited by factors such as the absorption capacity of the soil, soil pH and salinity, and metal phytotoxicity, differently to what happens to other heavy metals (Liet al., 2005). High metal concentration in kidneys and liver, as well as histopathological changes in kid- neys, were found in goats that were given lead acetate 50 mg/kg BW, cadmium chloride 10 mg/kg BW, or lead acetate 50 mg + cadmium chloride 10 mg/kg
BW, orally and daily for 42 days (Haneef et al., 1998). Milhaud et al. (2000) studied the transfer of Cd from feed to goat’s milk in lactating goats that received cadmium chloride 2 mg/kg BW or 4 mg/kg BW for 12 weeks. The pattern of Cd concentration in milk approached a steady-state condition after 10 weeks in both treated groups. The kinetics of Cd showed a non-linear relationship with Cd intake. In particular, the excretion of Cd in milk of goats fed 4 mg Cd/kg BW was threefold higher than that in goats fed 2 mg Cd/kg BW. This kinetic behaviour is explained by the high affinity of this heavy metal for some serum components, such as metallothioneins, which play an important role in metabolism and kinet- ics of the toxic metal (Luet al., 2005). Transfer of trace heavy metals to milk is a result of complex bio-mechanisms that require the activity of carrier proteins.
The pattern of Cd concentration in serum was similar to that in milk, even if the values were slightly higher. This suggests that the mammary gland did not act as a barrier to protect the suckling offspring, or other milk consumers, from exposure to the metal. Concentration of Cd in fresh curd was strongly associated with the con- centration of this heavy metal in the unprocessed milk and was about 3.5–5.5 times higher than that found in goat’s milk (Milhaudet al., 2000), similar to what is observed in cheese-making with sheep’s milk (Mehennaouiet al., 1999).