Polychlorinated biphenyls (PCBs) residues in milk from an agroindustrial zone of Tuxpan, Veracruz, Mexico

Chemosphere 89 (2012) 404–408

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Polychlorinated biphenyls (PCBs) residues in milk from an agroindustrial zone of Tuxpan, Veracruz, Mexico J. Jesús Pérez a, Salvador Vega y León b,⇑, Rey Gutiérrez b, Yanet López c, Roberto Faure c, Arturo Escobar c a

Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana Unidad Xochimilco, México, D.F., Mexico Universidad Autónoma Metropolitana Unidad Xochimilco (UAM-X), Departamento de Producción Agrícola y Animal, Laboratorio de Análisis Instrumental, México, D.F., Mexico c Centro Nacional de Sanidad Agropecuaria (CENSA), Dirección de Salud y Producción Animal, Departamento de Química-Farmacología, San José de las Lajas, Provincia Mayabeque, Cuba b

h i g h l i g h t s " There a contamination of cow milk by biphenyls polychlorinated in a tropical system. The presence of organic contaminants is due by punctual source. It

is the first research for this agroindustrial about organochlorine compounds. Production principal of milk is considered as organic product. The presence of high values of PCBs in milk will be a serious risk for population health.

a r t i c l e

i n f o

Article history: Received 15 November 2011 Received in revised form 16 April 2012 Accepted 19 May 2012 Available online 25 June 2012 Keywords: PCB Milk Mexico Residues

a b s t r a c t The coasts of the Gulf of Mexico are zones exposed to the exploration and exploitation of petroleum sources, and the products generated in agricultural zones may become contaminated by persistent organic pollutants (POPs). The objective of the present study was to evaluate the presence of polychlorinated biphenyl compounds (PCBs) in milk from dairy production units near sources of environmental pollutants. It was confirmed that the seven congeners of nondioxin-like PCBs (NDL-PCBs) are present in milk where compounds PCB101, PCB118, PCB153 and PCB180 appear in 100% of the samples analyzed, the rank of concentration for the sum of the seven congeners fluctuating between 2.6 and 26 ng g1 with a median of 6 ng g1. None of the samples surpassed the provisional value established by the EU of 40 ng g1 of milk fat for the sum of the seven congeners, indicator that was not affected by the season of the year (p < 0.05), whose median of 8.6 ng g1 and 6.3 ng g1 for rain and drought respectively. The concentrations of NDL-PCBs found in milk do not represent a problem for human health; however, they alert the existence of spontaneously generated, uncontrolled sources that may represent a potential danger for human and animal health. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction Human activities generate a great amount of chemical compounds in significant concentrations, which interact and contaminate the different ecosystems (Turrio-Baldassarri et al., 2009). Among the contaminants are the polychlorinated biphenyls (PCBs), the polycyclic aromatic hydrocarbons (PAHs) and the organochlorinated pesticides (OCPs), classified together as persistent organic pollutants (POPs) (Yarto et al., 2003; PNUMA, 2004). Due to their physiochemical properties, they migrate through the agro-alimentary chain accumulating in the lipid fractions of the segments that integrate this chain, which represents a risk for human and animal health, as the carcinogenic effects produced by some of the PAH ⇑ Corresponding author. E-mail address: [email protected] (Salvador Vega y León). 0045-6535/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2012.05.055

have been well documented (Delgado-Saborit et al., 2011), PCB (Miller-Pérez et al., 2009) and OCP (Thundiyil et al., 2007). More than 200 PCB are known and used mainly as dielectric fluids and heat exchangers in transformers and condensers, and there are different ways through which they are transferred to milk (Hirako, 2008). The presence of dioxin-like PCB in the human diet has been registered considering the analysis of 12 substitute non-ortho and non-ortho congeners, which are PCB77, PCB81, PCB126, PCB169, PCB105, PCB114, PCB118, PCB123, PCB156, PCB157, PCB167 and PCB189, establishing a toxic equivalent (TEQ) of 5.5 pg g1 of milk fat (EQT PCB-OMS) (UE, 2011). In the case of the nondioxin-like PCB (NDL-PCBs), the European Union (EU) has established provisional maximum levels of 100 ng g1 of milk fat for the sum of the seven congeners (EFSA, 2005; UE, 2006a,b) and recently was established a value of 40 ng g1 milk fat for the sum of six indicator

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PCBs (PCB 28, 52, 101, 138, 153 and 180) (EU 2011). A study carried out in diets for humans showed that the highest concentrations of dioxins and PCB appear in shellfish; however, milk and its derivates have the highest total toxic equivalents with 40% (Alcock, 2003). In Mexico, there are studies of the presence of PAH and PCB in soil, water and sediments, principally in the coastal zone of the Gulf of Mexico (Tamualipas, Veracruz, Tabasco and Campeche), given that it is an area that is highly exposed to the exploration and exploitation of petroleum (Bozada and Bejerano, 2006; Carvalho et al., 2009; Piazza et al., 2009). However, the available studies of the chemical safety of agricultural products in these agroindustrial zones are punctual and related only to the presence of OCP (Waliszewski et al., 1996; Waliszewski et al., 2004), not dealing with the PCB. Studies in other regions of the world have demonstrated the presence of PCB in milk fat in different species, which confirm that the animals exposed to these environmental contaminants excrete them through the milk (Thomas et al., 1998; Durand et al., 2008; Esposito et al., 2009). The objective of the present study was to evaluate the presence of PCB in milk from the municipality of Tuxpan, Veracruz, Mexico.

2. Materials and methods 2.1. Location of the study zone The municipality of Tuxpan Veracruz is located at 20°570 1800 latitude north and 97°230 5800 latitude west with an altitude of 14 m, bordering with the municipalities of Alamo-Temapache, Tamiahua, Tihualtlan, Poza Rica and with the Gulf of Mexico to the east. Its tropical climate is characterized by a mean temperature and rainfall of 24.9 °C and 1241 mm respectively. In the surroundings of the agricultural production units, there are two generating plants of electricity, a steel plant and others with petroleum activities. Two milk production units were studied, whose exploitation system is of extensive grazing (farm A) and the other semi-intensive (farm B) with a milk yield of 142 350 and 1095 000 L per year respectively.

2.2. Taking of samples Five hundred mL of milk sample were taken from the collection tank in each unit (A y B), monthly during one year (August 2009– 2010), a total of 12 samples per unit of production, considering the criteria of the Mexican norm (NMX, 2006) of the International Dairy Federation (FIL/IDF, 1995) and the general guidelines of sampling established by the CODEX Alimentarius (CODEX, 2004). Two periods of the year were considered; the rainy season (May–October) and the dry season (November–April).

2.3. Extraction and purification of fat Two-hundred fifty mililiter of a milk sample were placed in a volumetric flask of 500 mL and 250 mL of detergent solution were added (50 g of sodium hexametaphosphate and 24 mL of Tritón X100 dissolved in one liter of water). The flask was agitated vigorously and placed in a water bath at 90 °C, inverting the flask every 10 min until obtaining a clear separation of the fatty matter. The fat recovered from the milk samples was filtered at 50 °C through filter paper in the presence of anhydrous sodium sulfate. The samples were kept in glass tubes stored at 20 °C until the start of the analysis.

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2.4. Extraction and purification of PCB A chromatographic glass column (300  20 mm id) was conditioned, packed with 6 g of florisil (previously calcined at 550 °C for 6 h and maintained at 130 °C for 5 h, then was deactivated with 4% of H2O) and 1 g of anhydrous Na2SO4 (previously calcined at 600 °C for 6 h). The column was washed with 15 mL of hexane at a flow of 2 or 3 mL min1 and the eluate of the washing was discarded. 0.5 g of the fat dissolved in 5 mL of hexane was passed quantitatively to the column (rinsing the vial four times with a volume of 3 mL of hexane in each washing) and without allowing the column to dry, 72 mL of a mixture of hexane:dichloromethane 78:22 v/v were added. The eluate was collected in a flask of 125 mL, and brought to dryness in a retroevaporator, then the sample was reconstituted in 2 mL of the hexane:dichloromethane mixture and was quantitatively transferred to a conical tube. The eluate was dried under a flow of N2 and was kept at 20 °C until its analysis. The sample was reconstituted in 500 lL of hexane for its analysis in gas chromatograph. 2.5. Analysis of PCB A high resolution digital gas chromatograph model DANI Master CG was used with a PTV injector at 300 °C in the Splitless mode (split purge 40 mL min1 and split on 1 min, septum purge 5 mL min1). N2 was employed as gas carrier at a flow of 2.6 mL min1; the temperature of the ECD detector was 300 °C, and the N2 was used as auxiliary gas at 25 mL min1. The temperature of the oven was programmed as follows: temperature 1100 °C for 1 min with an increment of 3.5 °C min1 to 250 °C, temperature 2 at 250 °C for 2 min and a total time of the run of 46 min. The column employed was a TRB-5MS (30 m  0.32 mm id.  film thickness 0.25 lm). For the analysis of the chromatograms, the Software: CLARITY version 2.6 was used. 2.6. Identification and quantification A mixture of seven indicators of NDL-PCB (tri-PCB28, tetraPCB52, penta-PCB101, penta-PCB118, hexa-PCB138, hexa-PCB153 and hepta-PCB180) (RPCB-1JM Lot 435-65A), from the commercial firm CHEM SERVICE was used comparing the retention times and areas of the chromatographic signals. All of the chemical reactants employed were of reactive quality of the commercial firm Sigma and Merck for the analysis of residues. 3. Results and discussion Seven indicators of NDL-PCB (PCB28; PCB52; PCB101; PCB118; PCB153; PCB138; PCB180) were detected in milk samples. This finding confirms that their sum is a suitable marker to assess the level of exposure they are subjected, lactating animal and human species by these contaminants. Other studies have evaluated these same markers in milk from different species. (Focant et al., 2003; Costera et al., 2006; Esposito et al., 2009; Esposito et al., 2010; Konuspayeva et al., 2011). These aspects were confirmed under controlled studies and lactating cows to which the single dose of polychlorodibenzodioxins (PCDDs), polychlorodibenzofuranes (PCDFs) and polychlorobiphenyls (PCBs) was applied (Slob et al., 1995) or highly chlorinated compounds (Firestone et al., 1979). The transfer of PCBs in milk is a process governed mainly by the lipophilicity of congener and the lipid content present in the animal (McLachlan, 1993; Moser and McLachlan, 1999). On the other hand, an increase of chlorine in structure and coplanarity makes them less metabolized and causes a slow transport of congener

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and therefore a reduction in its excretion in milk (Fox et al., 1994; Fries, 1996). The compounds that exhibited the highest frequency in the present study were PCB101, PCB118, PCB153 and PCB180 with 100% (Table 1). None of the samples analyzed surpassed the provisional value established by the EU of 40 ng g1 of milk fat for the sum of seven congeners (EU 2011), the ranks being calculated in correspondence with those reported by researchers from other countries (Mamontova et al., 2007; Bayat et al., 2011). The median of the values obtained does not surpass the magnitude of 2 ng g1 of the milk fat for each congener, which may be due to the existence of a low concentration of these analytes in the ecosystem, the heptachlorobiphenyl PCB180 having the highest value of the median (1.6 ng g1) with respect to the rest of the NDL-PCB. This congener is the one containing the highest substitution of chlorine in its molecule and its coefficient of octanol– water partition (Kow) is 6.7–7, which increments its affinity for the liposoluble material (PNUMA, 2004; Fernandes et al., 2011). The other compounds detected in all the samples were PCB101, PCB118 and PCB153, whose coefficient of octanol:water fluctuated between 6.2 and 6.7, which is inferior to PCB180, thus they appear with a median of 0.5–0.9 ng g1 with respect to PCB180. These findings confirm that the transference of the PCB congeners is depends on the coefficient of partition octanol:water (Mclachlan, 1993; Miranda Filho et al., 2009; Kierkegaard et al., 2009). Studies that conducted a mass balance of PCB compounds in lactating cows concluded that the main route of exposure is through food, while feces and milk were the dominant elimination pathways of these persistent compounds (McLachlan et al., 1990; Mclachlan, 1993; Thomas et al., 1999; Kierkegaard et al., 2009). In our case, it did not conduct a mass balance study because the objective was to characterize the problem in the region and then to know the variables affecting in the contamination of persistent organochlorinated compounds in milk. In a validation study for the determination of PCB in biological matrices the value of 3.9 ng g1 was informed for milk fat where the congeners PCB118, PCB153, PCB138, PCB180 and PCB170 represented between 80 and 90% of the total PCB (Thomas et al., 1998). In another study with pasteurized milk, a higher concentration (7.56 ng g1) of PCB180 is reported with respect to its indicators NDL-PCB (Bayat et al., 2011). A study in the Republic of Kazakhstan in camel milk found that PCB52 and PCB101 indicators had a higher proportion relative to the sum of six indicator NDLPCBs (<60%) than that reported in Europe in cow milk (<10%), indicating the possible differences in the route of exposure to PCBs in the region studied (Konuspayeva et al., 2011). In the reports mentioned above, despite the existence of a consensus affirming that compounds with a high level of substitution of chlorine appear with higher frequency in milk of the exposed animals, there is still no reference compound that can be considered as an excretion marker, given that the factors influencing in its elimination in milk are very diverse. Therefore, the sum of those congeners with penta, hexa and biphenyl heptachlorine represents the indicator to evaluate exposure in animals. In the present work, the sum of these congeners reached 60% of the PCB detected. Fig. 1 shows the results of the two farms with no difference (p < 0.05) for PCBs indicators, which in any case, the sum of cong-

Fig. 1. Average values on the different congeners nondioxin-like PCBs in milk from two farm (A y B) in the region of Tuxpan Veracruz Mexico.

eners surpassed the value of 40 ng g1 milk fat. The maximum value of the sum was 11 and 26 ng g1 for A and B farms respectively. Values of the sum of PCB indicators in soil and grass in the region of Tuxpan appear in the ranges of 100–160 and 25–36 lg g1 respectively (unpublished data), corroborating aspects of animal exposure to these persistent organic pollutants, in other areas the State of Mexico has reported values of the sum of PCBs in a range of 47–11 000 ng g1 of soil (Rojas-Avelizapa et al., 2003), showing a chemical hazard of potential product contamination in agricultural farms near the industrial areas. The monitoring conducted in two farms in the region of Apulia in Italy found that the presence of PCBs in cow’s milk varied from region to region, being twice as high in the district of Bari (66.7 ng g1) as in Foggia (34.5 ng g1). Similar result was found with the analysis of organochlorine compounds where there was a trend to be higher in Bari, both of which had a higher environment contamination by the use of these products (Storelli et al., 2012). In an researcher carried out in the region of KwaZulu-Natal in South Africa, the presence of PCB was analyzed in milk from farms where the level of these contaminants (RPCB) in soil and air is high with figures of 109 ng g1 and 128 pg m3, respectively; and it was found that the PCB118, 101, 180, 52, 138 and 153 have the highest concentrations in milk, whose sum was 22 pg mL1 (Batterman et al., 2009). The above results indicate an association between PCB indicators present in milk with those appearing in the soil and grass, which together with the lipophilic property of rhese compounds, favor their excretion in milk (Lake et al., 2005; Mamontova et al., 2007; Batterman et al., 2009; Ounnas et al., 2010; Passuello et al., 2010). Fig. 2 shows the effect of the year seasons on the concentrations of NDL-PCB, not existing any difference (p < 0.05) between the rainy and dry seasons for each congener, presenting the highest average values of the indicators PCB52, PCB153 and PCB180 for both seasons with more than 70% of the sum of the seven indicators. A study carried out with cow’s milk during spring and autumn in the region of Siberia–Russia, the values referred were in the range of 3.9–44 ng g1 and 1.55–49 ng g1, respectively, for the sum of the seven congeners, not having differences between the seasons. The PCB118, PCB153, PCB138 and PCB132/105 are the

Table 1 Values of non-dioxin like PCBs present in milk from two production units of the region of Tuxpan, Veracruz, Mexico. ng g1 of Milk fat

Tri-CB28

Te-CB52

Pe-CB101

Pe-CB118

Hx-CB153

Hx-CB138

Hp-CB180

Minimum Maximum Average Median % Frequency

0.2 3.4 0.7 0.2 80

0.4 10.0 2.6 1.1 93.3

0.2 5.2 1.3 0.7 100

0.1 2.5 1.1 0.9 100

0.4 10.1 2.1 0.9 100

0.2 0.6 0.5 0.5 60

0.2 3.5 1.9 1.6 100

P PCBs 2.6 26.0 9.6 6.6

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limits of 100 ng g1 of fat established by the European Union, an do not represent a problem for human health. However, the values found demostrate the existence of other uncontrolled sources generated unintentionally, which may be a potential risk for human health if there is an increase in the values of these contaminants in agricultural products. Acknowledgements This research is part of the doctoral thesis of the first author, who is enrolled in a PhD program in Biological Sciences and Health, Universidad Autónoma Metropolitana Unidad Xochimilco. The authors acknowledge financial support from CONACyT (Mexico). References Fig. 2. Seasonal effect on the different congeners of non-dioxin like PCBs present in milk of the region of Tuxpan, Veracruz, Mexico.

majority with 60% of the total PCBs indicators. In winter, the levels of PCBs in milk from some farms increased due to the animals feeding pollute (land and roughage) during grazing, because the latter is highly deficient. (Mamontova et al., 2007). A study in the region of Andossi in Italy at an altitude of 1900 m showed the effect of seasonal and spatial variability of PCBs in vegetation and cow milk, where microclimatic conditions (temperature and air fluxes at a level soil) are capable of affecting the state of pollution in soil and grass (Tato et al., 2011). In another study carried out in air and soil of the different regions, it is indicated that the highest concentration of PCB coincides with the winter season with little rain (Batterman et al., 2009). In our study, there was the tendency having values of the PCB in the rainy season lower than those of the dry season, which may be due to a washing effect. That is, the rain washes the compounds deposited in the grass to the soil, being less contaminated at the moment consumption by the animals. This was confirmed when there is a higher concentration of PCB in soil in relation to the grass (unpublished data). Another important aspect is that PCB profiles in milk are different, coinciding only PCB153, an aspect that may be due to the animal metabolism and the days of lactation at the time of the studies (Thomas et al., 1999). There was not a uniform behavior in regard to the effect of season on contamination of PCB agricultural products, aspect that is related to multiple variables which contributed to this effect, such as anthropocentric activities. Researches carried out in dairy farms close to incineration plants in the province of Tuscany in Italy revealed that the neighboring zones presented higher levels of NDL-PCB in milk (0.71–2.9 pg WHO-TE/g of fat) with respect to the farms located in distant areas (0.52–0.59 pg WHO-TE/g of fat) (Ingelido et al., 2009). In our case, when not having main emission sources as incinerators and dielectric fluids in the region under study, it is confirmed the hypothesis that the levels of PCB should be within the permissible limits. However, from the levels found, the existence of other sources of unintentionally generated uncontrolled contamination is inferred. Thus, it is recommended to keep surveillance on the agricultural products and of the control program of the generation of dangerous residues from industry, fulfilling in this way with the obligations derived from the North American Free Trade Agreement (NAFTA) and the Stockholm agreement (Bozada and Bejerano, 2006). 4. Conclusions The levels of NDL-PCB in milk samples from the agroindustrial region of Tuxpan, Veracruz, Mexico, do not surpass the regulatory

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