Human Health Risk of Dietary Intake of Organochlorine Pesticide
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Food Chemistry 135 (2012) 1873–1893 Contents lists available at SciVerse ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem Human health risk of dietary intake of organochlorine pesticide residues in bovine meat and tissues from Veracruz, México ⇑ Violeta Pardío , David Martínez, Argel Flores, Dora Romero, Víctor Suárez, Karla López, Roxana Uscanga Faculty of Veterinary Medicine, Universidad Veracruzana, Veracruz, Mexico article info abstract Article history: Tissue distribution patterns of organochlorine pesticides in bovine carcasses varied significantly among Received 1 April 2012 seasons, geographic locations and tissues. The highest concentrations of RÀDDT during the dry season Received in revised form 10 June 2012 were detected in lungs from Paso de Ovejas (2,834.90 lg/kg lipid) and, during the rainy season, Lindane Accepted 24 June 2012 and RÀHCH in muscle and lung samples from Paso de Ovejas (995.80 and 1,690.10 lg/kg lipid). Esti- Available online 29 June 2012 mated daily intakes of cÀHCH and RÀDDT (3.35 and 1.22 lg/kg bw/day) through consumption of muscle tissues from Paso de Ovejas and Puente Nacional during the rainy season showed the highest contribu- Keywords: tion. During the rainy season the highest non-cancer Hazard Ratios estimated corresponded to cÀHCH Organochlorine pesticides (3.97) and R DDT (4.39) detected in muscle samples from Puente Nacional. The highest Hazard Ratios Bovine meat À Dietary intake of cancer risk to the 95th centile daily consumption through meat corresponded to p,p’-DDT from Alva- Health risk rado (7.76E + 06) and from Paso de Ovejas for cÀHCH (1.50E + 05) during rainy season. The results indi- cate potential non- and carcinogenic risks to consumer health through meat consumption. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction of their high lipid solubility, OCPs are deposited in adipose tissue and are excreted in milk (Pardío, Waliszewski, Landín, & Bautista, The use of persistent organochlorine pesticides (OCPs) in tropi- 2003). In bovine organisms after resorption, OCPs enter the liver cal countries has particular implications with regard to environ- and are metabolised slowly before they are released into the circu- mental and human exposure and food safety because high latory system and either finally deposited in the fat or excreted and temperatures in these regions allow the OCPs to volatilize and dis- passed onto the calf or to the consumer in milk (Jandacek & Tso, tribute uniformly in all parts of the environment (Manirakiza et al., 2001). According to MacLachlan (1996), a beef animal develops 2002). In Mexico, DDT was the principal insecticide used in malaria 100–150 kg of fat that accumulates the contaminant over its vector control programmes (Casas, Torres, Bown, Rodríguez, & Arre- 36 months lifespan as meat animals have no major fat excretion dondo, 1998; INE, 2002), routinely sprayed in the malaria- pathway and may never attain steady state levels in its 1–3 years endemic regions of Veracruz following WHO guidelines until lifespan (Rosenbaum, Mckone, & Jolliet, 2009). 2003 (SSA, 2006). Hexachlorocyclohexane (HCH) is a synthetic pes- Because of their high thermodynamic stability and lipid solubil- ticide with one isomer c-HCH, commonly referred to as Lindane, ity, OCPs bind to lipid components in animal tissues, becoming a still used in México in veterinary pest control. These contaminants major route of human exposure when consumed as food, contribut- are deposited through either dry gaseous, dry particle-bound, or ing to more than 90% of the daily exposure to these compounds. Pre- wet deposition to soil and plants, the first trophic level in the food vious studies have documented their bioaccumulation in the human terrestrial chain (Bolt & Degen, 2002), and due to their lipophilic body, especially in adipose tissue and breast milk (Covaci, de Boer, properties they bioaccumulate and biomagnify through the food Ryan, Voorspoels, & Schepens, 2002; Cruz, Lino, & Silveira, 2003; chain (Kalantzi et al., 2001; Vieira, Torres, & Malm, 2001). Animal Pardío et al., 1998; Snedeker, 2001; Waliszewski, Pardío, Chantiri, exposure may rise from direct treatment with pesticides, inhalation Infanzón & Rivera, 1996a; Zumbado et al., 2005). This tendency to of contaminated air, or through ingestion of contaminated forages, accumulate in body tissues, its long persistence and the acute health herbage and feedstuffs (Kalantzi et al., 2001; Semeena, Feichter, & risks of OCPs, have raised concerns about possible human health im- Lammel, 2005; Willett, O’Donnell, Durst, & Kurz, 1993). Because pacts due to low, but chronic, exposure from dietary intake. Organo- chlorine pesticides have been considered as ‘endocrine—disrupting ⇑ Corresponding author. Address: Laboratory of Toxicology, Faculty of Veterinary chemicals’ and carcinogenic substances (Amaral-Mendes, 2002; Medicine, Universidad Veracruzana, Avenida Miguel Ángel de Quevedo s/n, Colonia Kavlock, 1996; Lemaire, Terouanne, Mauvais, Michel, & Rahmani, Unidad Veracruzana, Veracruz 91710, Mexico. Tel.: +52 229 9342075x24125; fax: 2004; Witorsch, 2002). DDE inhibits androgen binding to the +52 229 9342075x24104. androgen receptor, whereas DDT has potent estrogenic activity in E-mail addresses: [email protected], [email protected] (V. Pardío). 0308-8146/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2012.06.079 1874 V. Pardío et al. / Food Chemistry 135 (2012) 1873–1893 mammals (Kelce, Gray, & Wilson, 1998; Kelce et al., 1995; Son- sue, were collected at random from 24 carcasses of healthy male nenschein & Soto, 1998). Recent epidemiological studies indicate steers that were 12–16 months old; each group of 3 animals slaugh- that some of these compounds may influence the concentrations tered at the slaughter house located in Vargas, Veracruz, México, of thyroid hormones (Meeker, Altshul, & Hauser, 2007), and the pos- were sampled during two sampling periods. The cattle were fed a sible association between exposure to DDT and various types of balanced diet and tap water ad libitum as part of routine manage- cancers in humans, including leukaemia, prostate, brain, and lym- ment practices used at each production center. Livestock originated phopoietic cancers, non-Hodgkins lymphoma and multiple myelo- from four extensive breeding stock on commercial bovine produc- ma, have been studied extensively (Beard, 2006; Dreiher & ing farms located in the south-west region from the central agrarian Kordysh, 2006; IARC, 2008; Quintana et al., 2004). Cox, Niskar, Nara- zone of Veracruz, Mexico showed in Fig. 1: Puente Nacional (PN) yan, and Marcus (2007) found among Mexican Americans residing (19°200 N, 95°080 W and 100 m over sea level), Alvarado (ALV) in the southerwestern United States with elevated serum glucose (18°460 N, 95°460 W and 10 m over sea level), Paso de Ovejas (PO) levels that self-reported diabetes was significantly associated with (19°170 N, 95°460 W and 40 m over sea level), and Manlio Fabio Alta- serum levels of bÀHCH, p,p0-DDT, and p,p0-DDE, suggesting that mirano (MFA) (19°060 N, 96°200 W and 40 m over sea level). The cli- higher serum levels of certain organochlorine pesticides may be mate in this region is characterised by a dry season (from November associated with increased prevalence of diabetes. The impacts of to April) and a rainy season (from May to October) (INEGI, 2008). prenatal exposure to DDT on children’s neurodevelopment have Three samples (500 g each) of each tissue -muscle, subcutane- also been investigated; Eskenazi et al. (2006) found an association ous adipose tissue, spinal marrow, liver, heart, lung and kidney, with delays in neurodevelopment during early childhood. were individually wrapped in pre-treated aluminium foil immedi- These compounds also have the potential to compromise the ately after collection and packed separately in ziplock plastic bags health and productivity of domestic animals. Monitoring OCPs in and transported fresh in coolers to the Toxicology laboratory of the animal tissues collected from different locations is important be- Veterinary Faculty. Muscle and tissue samples were analysed with- cause it provides useful information concerning the extent of pol- in 24 h or kept at À25 °C until extraction was carried out. Prior to lution trends in relation to local origin, it helps to elucidate the the extraction, all glassware were properly washed with detergent spatial variation in contamination patterns, and to assess the (free of chlorinated hydrocarbons) and rinsed with distilled water. health risks associated with the consumption of contaminated food The water was removed with acetone and the acetone with petro- from animals (Jevsnik, Cerkvenik, & Doganoc, 2004). It is estimated leum ether and glassware then heated in an oven at 400° C for 4 h that meat and meat products contribute to 15–20% of OCPs when to avoid any contamination of pesticides (UNEP, 1988). All chemi- compared the other foodstuffs. Meat and meat products are impor- cals were analytical grade and obtained from Merck (Darmstadt, tant foods and there are various reports on the residual levels of Germany), J.T. Baker and Sigma–Aldrich Company (St. Louis, MO, OCPs in these products over the world (Barkatina et al., 1999; USA) and used without further purification. Glynn et al., 2000; Hashemy-Tonkabony et al., 1981; Manirakiza et al., 2002; Osibanjo & Adeyeye, 1997; Schecter, Cramer, Boggess, 2.2. Determination of organochlorine pesticide