Serum concentrations of p,p′-dichlorodiphenyltrichloroethane (p,p′-DDE) in a sample of agricultural workers from Bolivia

Chemosphere xxx (2013) xxx–xxx

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Serum concentrations of p,p0 -dichlorodiphenyltrichloroethane (p,p0 -DDE) in a sample of agricultural workers from Bolivia Luis A. Mercado a,⇑, Sara M. Freille a, Jasmin S. Vaca-Pereira a, Miriam Cuellar a, Lizbeth Flores a, Elaine Mutch d, Nicolas Olea b,c, Juan P. Arrebola b,c,⇑ a

Instituto de Investigaciones de la Facultad de Ciencias Farmacéuticas y Bioquímicas, Universidad Autónoma Gabriel René Moreno, Calle México s/n, Santa Cruz de la Sierra, Bolivia Laboratory of Medical Investigations, San Cecilio University Hospital, University of Granada, 18071 Granada, Spain Consortium for Biomedical Research in Epidemiology and Public Health (CIBER en Epidemiología y Salud Pública-CIBERESP), Spain d Institute of Cellular Medicine, University of Newcastle upon Tyne NE2 4HH, UK b c

h i g h l i g h t s " Serum p,p0 -DDE and o,p0 -DDT were quantified in 70 agricultural workers. " p,p0 -DDE showed a median concentration of 19.7 ng mL

1

(4788.7 ng/g lipid).

" o,p0 -DDT was only detected in 3 samples (4.3%). " p,p0 -DDE was associated with time of residence, hygiene habit and body mass index.

a r t i c l e

i n f o

Article history: Received 23 March 2012 Received in revised form 30 November 2012 Accepted 15 December 2012 Available online xxxx Keywords: Dichlorodiphenyltrichloroethane p,p0 -Dichlorodiphenyldichloroethylene Serum Agricultural worker Occupational exposure Exposure predictor

a b s t r a c t Organochlorine pesticide p,p0 -dichlorodiphenyltrichloroethane (DDT) is still used for vector control in several tropical and subtropical areas of South America and there is evidence of recent illegal use in agriculture. Its main breakdown product in the environment and living organisms is p,p0 -dichlorodiphenyldichloroethylene (p,p0 -DDE), which is considered a marker of past exposure to DDT. The aim of the present study was to assess human exposure to p,p0 -DDE in a sample of agricultural farmers from three rural communities in eastern Bolivia. In addition, o,p0 -DDT was analyzed as a surrogate of a potential ongoing exposure to the pesticide. Face-to-face questionnaires were performed, and serum samples were analyzed by high-resolution gas chromatography with mass spectrometry. p,p0 -DDE was found in 100% of the samples, with a median concentration of 19.7 ng mL1 (4788.7 ng/g lipid), while o,p0 -DDT was detected in 3 samples (4.3%). Serum p,p0 -DDE concentrations were associated with time of residence in the study area, personal hygiene after work, and body mass index in adjusted multinomial logistic regression models with tertiles of p,p0 -DDE as the dependent variable. The present results revealed high levels of exposure to p,p0 -DDE, which might be derived from a heavily polluted local environment and past occupational exposure. These findings deserve further attention due to the potential associated health risks and point to the need for the continuous monitoring of these populations. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction 0

Abbreviations: DDT, p,p -dichlorodiphenyltrichloroethane; OCP, organochlorine pesticide; p,p0 -DDE, p,p0 -dichlorodiphenyldichloroethylene; POP, persistent organic pollutant; BMI, body mass index (BMI); OR, odds ratio; LD, limit of detection. ⇑ Corresponding authors. Addresses: Instituto de Investigaciones de la Facultad de Ciencias Farmacéuticas y Bioquímicas, Universidad Autónoma Gabriel René Moreno, Calle México s/n, Santa Cruz de la Sierra, Bolivia. Tel.: +591 70079930 (L.A. Mercado), Laboratory of Medical Investigations, San Cecilio University Hospital, University of Granada, 18071 Granada, Spain. Tel.: +34 958 242864; fax: +34 958 249953 (J.P. Arrebola). E-mail addresses: [email protected] (L.A. Mercado), [email protected] (J.P. Arrebola).

Pesticide p,p0 -dichlorodiphenyltrichloroethane (DDT, CAS # 107917-42-0) was the first organochlorine pesticide (OCP) to be marketed and was extensively used in agriculture and public health campaigns in most countries until the 1970s. However, DDT is still permitted for vector control (e.g., malaria, dengue, leishmaniasis, and Chagas disease) in several tropical and subtropical areas of South America and other regions of the planet (UNEP, 2002), accounting for an estimated consumption of 4–5000 metric ton year1

0045-6535/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2012.12.023

Please cite this article in press as: Mercado, L.A., et al. Serum concentrations of p,p0 -dichlorodiphenyltrichloroethane (p,p0 -DDE) in a sample of agricultural workers from Bolivia. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2012.12.023

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L.A. Mercado et al. / Chemosphere xxx (2013) xxx–xxx

(active ingredient) worldwide (van den Berg, 2009). DDT started to be used in South America in the 1940s and was prohibited in Bolivia in 1996 due to its potential threat to human health. Nevertheless, illegal use of DDT in the country has been reported since that date (UNEP, 2002). DDT has a half-life of 2–15 years in the environment (EPA, 1989), and p,p0 -dichlorodiphenyldichloroethylene (p,p0 -DDE, CAS # 82413-20-5) is its main breakdown product in the environment and living organisms (ATSDR, 2002). p,p0 -DDE tends to persist for much longer in comparison to the parent compound and is considered a marker of past exposure to DDT (World Health Organization, 1989). Both DDT and DDE are persistent organic pollutants (POPs), i.e. synthetic chemicals that are highly lipophilic and resistant to biodegradation (Porta et al., 2008; Rollin et al., 2009). Exposure to p,p0 -DDE in the general population occurs mainly through diet, but historical occupational exposure to DDT can also be of importance (Cooper et al., 2004). A number of health effects potentially derived from human exposure have been described, including certain types of cancer, leukemia, diabetes, neurodevelopmental disorders, and impaired fertility (Garabrant et al., 1992; Eriksson and Talts, 2000; Snedeker, 2001; Chen and Rogan, 2003; Beard, 2006; Ribas-Fito et al., 2006; Cox et al., 2007; Arrebola et al., 2013). However, the relationship between long-term exposure to these pollutants and health outcomes remains poorly understood (Porta et al., 2008). The aim of the present study was to assess human exposure to p,p0 -DDE in a group of agricultural farmers from three agricultural communities in eastern Bolivia.

The biological samples and independent variables were collected between November 2010 and April 2011. Information on potential predictors of exposure was gathered from an ad hoc questionnaire completed by each participant and conducted faceto-face by two trained interviewers. Participants’ height and weight were measured and their body mass index (BMI) was calculated as weight/height squared (kg m2). Smoking habit and consumption of alcohol (beer, wine and liquor) were measured as no. of cigs week1 and no. of bottles week1, respectively. The variable ‘‘current use of OCPs’’ (yes/no) was considered in the analyses because there is evidence of the illegal use of DDT and other OCPs, such as dicofol, which is a well-known source of indirect exposure to DDT (Guo et al., 2009). This information was extracted from the questionnaires, in which the participants were asked about the brands of pesticides in use at this time. Characteristics of the study population are summarized in Table 1. There were 46 (66%) men, 11 (15.5%) subjects were current smokers, 25 (43.9%) declared habitually using protection against pesticide exposure at their workplace, and 39 subjects (54.9%) reported taking a daily bath after finishing work. A total of 45 subjects (64%) reported being involved in the preparation or application of pesticide mixtures, and 19 (26.8%) were using OCPs at the time of sample collection. All subjects declared that DDT was used at their workplaces until 2000. The study was approved by the ethics committee of the Universidad Autónoma Gabriel René Moreno, Bolivia.

2. Materials and methods

Blood samples (10 mL, n = 70) were collected and immediately coded and stored at 80 °C until chemical analysis. The chemical extraction procedure to isolate analytes from serum samples has been reported elsewhere (Martinez Vidal et al., 2002; Moreno-Frias et al., 2004). From each serum sample, 4 mL was extracted with acidified diethyl ether and n-hexane, and the cleaned-up extract was eluted through a solid phase silica extraction column (Sep Pack, Waters). Residues of p,p0 -DDE and o,p0 -DDT were quantified by highresolution gas chromatography coupled with mass spectrometry, using a 6890 Agilent gas chromatograph with a 5590 quadruple mass selective detector (Agilent Technologies, Wilmington, USA). p,p0 -Dichlorobenzophenone was used as internal standard. Limits of detection were considered the smallest amount of analyte giving a signal-to-noise ratio P 3 and were set at 0.1 ng mL1 for each analyte. Recovery rates ranged from 70% to 98%. Total lipid content in serum samples was calculated as described by Phillips et al. (1989). OCP concentrations were expressed on both wet-basis (ng mL1) and lipid-basis (ng/g lipid), calculating the latter by dividing the wet-basis concentration by the total lipids in each sample.

2.1. Study area Agricultural activity in the study area is mainly based on independent farmers who work their own plots of land and are grouped in local communities. Study subjects were recruited from among agricultural workers residing in the communities of Algodonal, Aguas Claras, and La Junta, located in the subtropical region of Santa Cruz, Eastern Bolivia. These communities have an estimated population of 679 inhabitants and are situated around 170 km from the city of Santa Cruz de la Sierra (1 500 000 inhabitants). Their economy is based on agriculture, and the area is considered one of the main suppliers of agricultural produce to Santa Cruz de la Sierra. The main crop in the area is tomatoes, followed by other vegetables (e.g., potatoes and red peppers). According to reports by the workers, the most widely used pesticides at the time of the study were organophosphates (Chlorpyrifos, Methamidophos, Monocrotophos and Glyphosate), pyrethroids (Cypermethrin and Cyhalothrin), carbamates (Methomyl and Mancozeb), and one OCP (Dicofol). 2.2. Study population According to reports from the local community authorities, the universe of agricultural workers in the study area was estimated to be 225. After contacting the workers through their local leaders, the research team organized meetings with them in each community. Inclusion criteria were: age over 18 years and residence in the study area for at least 5 years. A total of 179 (79.5%) agricultural workers attended the meetings and agreed to become study participants, and 75 of these were selected by simple random sampling. Out of these individuals, five (two males and three females) were excluded from the study for missing their appointment for the sample extraction; therefore, 70 workers were finally included in the study. All participants signed their informed consent.

2.3. Sampling and chemical analysis

Table 1 Characteristics of the study population. Median

Age BMI (kg m2) Time of residence (years) Distance from residence to agricultural site (m) Recent weight loss (kg) Smoking habit (No. cigs week1) No. of children Cholesterol (mg dL1) Triglycerides (mg dL1) Total serum lipids (mg dL1)

42.5 24.0 20.0 300.0 0.0 0.0 3.0 160.0 106.0 4.8

Percentiles 25

75

30.0 22.7 6.5 100.0 0.0 0.0 1.3 140.3 69.0 4.8

50.3 26.3 39.0 1000.0 3.0 0.0 5.0 194.8 152.3 5.0

Please cite this article in press as: Mercado, L.A., et al. Serum concentrations of p,p0 -dichlorodiphenyltrichloroethane (p,p0 -DDE) in a sample of agricultural workers from Bolivia. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2012.12.023

L.A. Mercado et al. / Chemosphere xxx (2013) xxx–xxx Table 2 Concentrations of p,p0 -DDE in serum from Bolivian agricultural workers. p,p0 -DDE

>LD (%)

Percentiles 25th

50th

75th

95th

70 (100%)

4.75 1197.76

19.75 4788.75

54.97 12403.87

169.68 35131.24

Men ng mL1 ng/g Lipid

46 (100%)

7.73 1242.24

31.76 5925.43

81.25 15116.72

196.79 40742.58

Women ng mL1 ng/g Lipid

24 (100%)

4.00 873.37

9.34 2024.41

33.67 6972.24

139.34 28792.56

Total ng mL1 ng/g Lipid

LD: Limit of detection.

A double-blinded procedure was followed, and none of the chemical analysts or statisticians was aware of the identity of any study subject. 2.4. Statistical methods Median and 25th–75th percentiles were calculated for the continuous independent variables and p,p0 -DDE concentrations. Potential predictors of wet serum concentrations of p,p0 -DDE were assessed by using multinomial logistic regression models with tertiles of serum p,p0 -DDE as dependent variable, and odds ratios (ORs) and their 95% confidence intervals were calculated. In order to control for potential confounding effects, models were sequentially adjusted for sex and age. Models calculated using wet-basis and lipid-basis concentrations showed only minor differences in the results, therefore only those based on wet-basis concentrations are shown. Wet-basis concentrations were also adjusted for ‘‘total lipids’’ (g L1). 3. Results and discussion This study represents a continuation of our research line on the characterization of human exposure to environmental pollutants in Bolivia from different perspectives (Arrebola et al., 2012a,b,c). In the present cohort of Bolivian agricultural workers, all samples (100%) showed detectable levels of p,p0 -DDE, with a median concentration of 19.7 ng mL1 (4788.7 ng/g lipid). The distribution of the concentrations is shown in Table 2 and Fig. 1. o,p0 -DDT was detected only in three (4.3%) samples. Exposure to p,p0 -DDE was very

3

high in these workers in comparison to findings in the USA or Europe (Petrik et al., 2006; CDC, 2009; Porta et al., 2012) and were comparable to reports in heavily exposed populations of South Africa and Mexico, where the pesticide DDT is currently used in public health campaigns (Minelli and Ribeiro, 1996; Waliszewski et al., 2000; Rollin et al., 2009). A study of malaria control workers in Brazil showed a change in median p,p0 -DDE serum concentrations from 119.8 in 1997 to 27.7 ng mL1 in 2001 (Ferreira et al., 2011), and the latter is relatively close to the present finding. Another study of malaria control workers in South Africa in the 1990s also reported levels above 100 ng mL1 (Bouwman et al., 1994). The present study population shows a very different pattern of exposure to that observed in an urban population from Santa Cruz de la Sierra, Bolivia (Arrebola et al., 2012a,b), whose serum p,p0 -DDE concentrations were markedly lower (geometric mean = 1.2 ng mL1; 267.4 ng/g lipid). Age- and sex-adjusted multinomial logistic regression analyses (Table 3) showed that time of residence in the present study area was associated with the serum p,p-DDE concentrations, with an increase of 5–7% in the risk of being in the 2nd or 3rd tertiles of exposure for each additional year of residence. Longer residence is also likely to imply a longer time of occupational exposure through agricultural activity. The difference in exposure between inhabitants of this agricultural area and the nearby city of Santa Cruz de la Sierra likely indicates a heavily DDT-polluted local environment as well as the past occupational exposure of the farmers. Studies in other countries have found high levels of DDT isomers and metabolites in people residing close to areas of intensive pesticide application (Rollin et al., 2009; Waliszewski et al., 2010). o,p0 -DDT was chosen as a surrogate for contemporary exposure, because this isomer is commonly detected in serum from currently exposed subjects (Minelli and Ribeiro, 1996; Rollin et al., 2009), being more rapidly metabolized than p,p0 -DDT and p,p0 -DDE and being only a minor component (around 15%) of commercial formulations of the pesticide (Cohn et al., 2010). Although there is evidence of illegal trading of DDT in Bolivia (UNEP, 2002), only a few samples showed detectable levels of o,p0 -DDT, suggesting that its current use may not be widespread. This is consistent with the reports of the workers that they had not used the pesticide DDT since 2000 (4 years after its official prohibition). The borderline significant association found between the BMI and serum p,p0 -DDE concentrations in this population may be explained by dietary exposure, in line with reports that a high proportion of human exposure to POPs is through diet (Gunderson,

Fig. 1. p,p0 -DDE concentrations in serum from Bolivian agricultural workers (n = 70). This figure shows a box-plot graph with the distribution of p,p0 -DDE concentrations in serum from the agricultural workers expressed in wet- and lipid-basis.

Please cite this article in press as: Mercado, L.A., et al. Serum concentrations of p,p0 -dichlorodiphenyltrichloroethane (p,p0 -DDE) in a sample of agricultural workers from Bolivia. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2012.12.023

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L.A. Mercado et al. / Chemosphere xxx (2013) xxx–xxx

Table 3 Multivariate multinomial logistic regression for predictors of p,p0 -DDE tertiles in agricultural workers. Tertilee

Crude modela SE

OR

95% Cl

Sex = females 2 0.80 3 0.95

0.61 0.63

0.45 0.39

0.14 0.11

Age (years) 2 0.01 3 0.01

0.02 0.02

1.01 1.01

Time of residence (years) 2 0.05 0.02 3 0.06 0.02

a

c d e

Adjusted modelc

b

SE

OR

95% Cl

1.50 1.33

– –

– –

– –

– –

0.97 0.97

1.05 1.06

0.01 0.02

0.02 0.02

1.01 1.02

1.05 1.07

1.01 1.02

1.10 1.11

0.05 0.06

0.02 0.02

Residence > 1 km agriculture 2 0.59 0.60 0.55 3 0.17 0.59 1.19

0.17 0.37

1.81 3.80

0.40 0.46

BMI (kg m2) 2 0.08 3 0.08

b

b

Adjusted modelb

Adjusted modeld

b

SE

OR

95% Cl

b

SE

OR

95% Cl

– –

0.84 1.01

0.62 0.64

2.30 2.74

0.69 0.78

7.75 9.62

– –

– –

– –

– –

– –

0.97 0.98

1.05 1.06

– –

– –

– –

– –

– –

– –

– –

– –

– –

– –

1.05 1.06

1.01 1.02

1.09 1.11

0.06 0.07

0.02 0.02

1.06 1.07

1.01 1.02

1.11 1.12

0.05 0.07

0.02 0.02

1.05 1.07

1.01 1.02

1.10 1.12

0.63 0.63

0.67 1.59

0.19 0.46

2.33 5.50

0.63 0.12

0.61 0.60

0.53 1.13

0.16 0.35

1.76 3.67

0.44 0.41

0.64 0.64

0.64 1.51

0.18 0.43

2.25 5.30

0.06 0.06

1.08 1.08

0.96 0.96

1.22 1.23

0.11 0.11

0.07 0.07

1.11 1.12

0.97 0.97

1.27 1.28

0.08 0.08

0.06 0.06

1.08 1.08

0.96 0.95

1.22 1.22

0.10 0.10

0.07 0.07

1.11 1.11

0.97 0.97

1.27 1.27

Recent weight loss = yes 2 0.43 0.59 3 0.54 0.61

0.65 1.72

0.21 0.53

2.06 5.64

0.51 0.46

0.60 0.62

0.60 1.58

0.18 0.47

1.95 5.28

0.48 0.50

0.60 0.61

0.62 1.64

0.19 0.49

1.99 5.44

0.60 0.36

0.62 0.63

0.55 1.44

0.16 0.42

1.83 4.94

Recent weight loss (kg) 2 0.11 0.12 3 0.07 0.12

1.12 1.07

0.89 0.85

1.40 1.35

0.11 0.07

0.12 0.12

1.11 1.07

0.88 0.84

1.40 1.36

0.11 0.07

0.12 0.12

1.12 1.08

0.89 0.85

1.41 1.36

0.11 0.07

0.12 0.13

1.12 1.07

0.88 0.84

1.42 1.37

Current smoker = yes 2 1.99 1.13 3 1.56 1.17

0.14 0.21

0.01 0.02

1.27 2.07

1.78 1.24

1.17 1.20

0.17 0.29

0.02 0.03

1.67 3.03

1.96 1.50

1.14 1.18

0.14 0.22

0.02 0.02

1.32 2.23

1.73 1.13

1.18 1.21

0.18 0.32

0.02 0.03

1.80 3.46

Smoking habit (cigs week1) 2 0.04 0.04 1.04 3 0.03 0.04 1.03

0.96 0.94

1.13 1.12

0.03 0.02

0.04 0.04

1.03 1.02

0.95 0.93

1.12 1.11

0.04 0.03

0.04 0.05

1.04 1.03

0.95 0.94

1.13 1.12

0.03 0.01

0.04 0.04

1.03 1.01

0.95 0.93

1.11 1.10

Beer consumption = yes 2 0.05 0.11 3 0.08 0.10

1.05 1.08

0.85 0.88

1.29 1.33

0.01 0.02

0.11 0.11

0.99 1.02

0.79 0.82

1.24 1.27

0.05 0.09

0.11 0.11

1.06 1.10

0.86 0.89

1.30 1.35

0.00 0.03

0.11 0.11

1.00 1.03

0.80 0.83

1.25 1.29

Wine consumption = yes 2 0.28 0.45 3 0.41 0.54

0.76 0.67

0.31 0.23

1.82 1.92

0.37 0.52

0.46 0.56

0.69 0.59

0.28 0.20

1.71 1.80

0.26 0.38

0.45 0.54

0.77 0.69

0.32 0.24

1.87 1.99

0.35 0.49

0.46 0.57

0.71 0.62

0.28 0.20

1.75 1.86

Liquor consumption = yes 2 0.83 0.87 3 0.77 0.87

2.30 2.16

0.42 0.39

12.56 11.84

0.67 0.59

0.81 0.82

1.96 1.81

0.40 0.37

9.64 8.96

0.84 0.77

0.89 0.89

2.32 2.16

0.40 0.38

13.27 12.43

0.66 0.58

0.84 0.84

1.94 1.78

0.38 0.35

9.98 9.19

Daily bath after work = no 2 0.20 0.63 1.22 3 0.96 0.63 2.60

0.36 0.76

4.16 8.88

0.67 1.70

0.75 0.78

1.95 5.49

0.45 1.20

8.47 25.20

0.19 0.95

0.64 0.63

1.20 2.58

0.35 0.74

4.18 8.91

1.10 1.84

0.01 0.01

3.01 6.31

2.96 6.21

3.06 6.41

Habitually use protection against pesticides = yes 2 0.54 0.64 0.58 0.17 2.06 3 0.30 0.62 1.35 0.40 4.54

0.54 0.32

0.65 0.62

0.58 1.38

0.16 0.41

2.08 4.69

0.84 0.05

0.63 0.59

0.43 0.95

0.13 0.30

1.48 3.02

0.19 0.30

0.70 0.70

0.83 0.74

0.21 0.19

3.27 2.90

Current use of OCPs = yes 2 0.05 0.67 3 0.36 0.77

0.71 1.25

0.86 0.95

2.04 3.50

0.37 0.55

11.06 22.31

0.06 0.30

0.67 0.78

0.95 1.34

0.25 0.29

3.53 6.23

0.70 1.20

0.87 0.95

2.02 3.31

0.37 0.51

10.98 21.41

0.95 1.43

0.26 0.32

3.52 6.49

Adjusted for total serum lipids. Adjusted for total serum lipids and sex. Adjusted for total serum lipids and age. Adjusted for total serum lipids, sex and age. Reference category = 1st tertile; OR: odds ratio; SE: standard error; CI: confidence interval.

1995). However, occupational exposure is known to be of great importance in agricultural workers (Cooper et al., 2004), especially in developing countries, where inadequate controls can lead to a higher use of illegal pesticides (el Sebae, 1993). Interestingly, study participants who did not take a daily bath after work showed an OR of 3 for the 2nd tertile and an OR of 6.3 for the 3rd tertile of exposure to p,p0 -DDE. These results indicate the need for further action to reduce human exposure, including educational programs. Although we only gathered information on current hygiene habits, we assumed that these were unlikely to have changed significantly over the period of residence in the area (median of 20 years). We found ORs > 2 for females in the second and third tertiles of exposure in the adjusted model. The results were not statistically

significant but indicate an association that might be evident in larger population samples. The fact that women are at higher risk of exposure to environmental pollutants, especially in developing countries, has been reported elsewhere (Kunstadter et al., 2001; London et al., 2002; Garcia, 2003; Arrebola et al., 2009; Salihovic et al., 2012). Several reasons have been suggested for this finding, including gender-related differences in cytochrome P450 metabolism (McTernan et al., 2002) and in the perception of potential occupational exposure (Joffe, 1992). Despite the limited sample size, the present study shows a very high exposure to p,p0 -DDE in the study population, which is of special concern given the reported associated health risks, such as the greater likelihood of preterm birth and small-for-gestational-age

Please cite this article in press as: Mercado, L.A., et al. Serum concentrations of p,p0 -dichlorodiphenyltrichloroethane (p,p0 -DDE) in a sample of agricultural workers from Bolivia. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2012.12.023

L.A. Mercado et al. / Chemosphere xxx (2013) xxx–xxx

babies in women with serum concentrations > 10 ng mL1 (Longnecker et al., 2001), decreased immunoglobulin A levels in male farmers with serum concentrations P 6.0 lg L1 (Cooper et al., 2004), and of testicular germ cell tumors in patients with serum p,p0 -DDE concentrations > 390 ng/g lipid (McGlynn et al., 2008). These cut-off points are below the median concentrations observed in our cohort of agricultural workers, emphasizing the need for further research on exposure-related health outcomes. 4. Conclusions The study population showed very high concentrations of p,p0 -DDE in their adipose tissue that are likely to be caused by a contaminated local environment due to the intense historical use of pesticides in the region. Acknowledgements The study was partially supported by the ‘‘Impuesto Directo a Hidrocarburos’’ (IDH) of the Government of Bolivia, the EU Commission (CONTAMED FP7-ENV-212502), the Spanish Ministry of Health (EUS2008-03574), Instituto de Salud Carlos III (FIS PI11/ 0610), and the Regional Government of Andalusia–Spain (Grant Numbers P09-CTS-5488 Project of Excellence, and SAS PI-06752010). Dr. J.P. Arrebola is under contract with the PTA-MICINN program (Spanish Ministry of Science and Innovation). The authors are grateful to Richard Davies for editorial assistance. The authors are indebted to all of the agricultural workers who took part in the study, without whom this work would not have been possible. References Arrebola, J.P., Martin-Olmedo, P., Fernandez, M.F., Sanchez-Cantalejo, E., JimenezRios, J.A., Torne, P., Porta, M., Olea, N., 2009. Predictors of concentrations of hexachlorobenzene in human adipose tissue: a multivariate analysis by gender in Southern Spain. Environ. Int. 35, 27–32. Arrebola, J.P., Cuellar, M., Claure, E., Quevedo, M., Antelo, S.R., Mutch, E., Ramirez, E., Fernandez, M.F., Olea, N., Mercado, L.A., 2012a. Concentrations of organochlorine pesticides and polychlorinated biphenyls in human serum and adipose tissue from Bolivia. Environ. Res. 112, 40–47. Arrebola, J.P., Mutch, E., Rivero, M., Choque, A., Silvestre, S., Olea, N., Ocaña-Riola, R., Mercado, L.A., 2012b. Contribution of sociodemographic characteristics, occupation, diet and lifestyle to DDT and DDE concentrations in serum and adipose tissue from a Bolivian cohort. Environ. Int. 38, 54–61. Arrebola, J.P., Mutch, E., Cuellar, M., Quevedo, M., Claure, E., Mejia, L.M., FernandezRodriguez, M., Freire, C., Olea, N., Mercado, L.A., 2012c. Factors influencing combined exposure to three indicator polychlorinated biphenyls in an adult cohort from Bolivia. Environ. Res. 116, 17–25. Arrebola, J.P., Pumarega, J., Gasull, M, Fernandez, M.F., Martin-Olmedo, P., MolinaMolina, J.M., Fernández-Rodríguez, M., Porta, M., Olea, N., 2013. Adipose tissue concentrations of persistent organic pollutants and prevalence of type 2 diabetes in adults from Southern Spain. Environ. Res., in press, http:// dx.doi.org/10.1016/j.envres.2012.12.001. ATSDR, 2002. Toxicological profile for DDT, DDE, and DDD. Agency for Toxic Substances and Disease Registry, US Department of Health and Human Service. Beard, J., 2006. DDT and human health. Sci. Total Environ. 355, 78–89. Bouwman, H., Becker, P.J., Schutte, C.H., 1994. Malaria control and longitudinal changes in levels of DDT and its metabolites in human serum from KwaZulu. Bull. World Health Org. 72, 921–930. CDC, 2009. Fourth National Report on Human Exposure to Environmental Chemicals. Centers for Disease Control and Prevention. Atlanta. Chen, A., Rogan, W.J., 2003. Nonmalarial infant deaths and DDT use for malaria control. Emerg. Infect. Dis. 9, 960–964. Cohn, B.A., Cirillo, P.M., Christianson, R.E., 2010. Prenatal DDT exposure and testicular cancer: a nested case-control study. Arch. Environ. Occ. Health 65, 127–134. Cooper, G.S., Martin, S.A., Longnecker, M.P., Sandler, D.P., Germolec, D.R., 2004. Associations between plasma DDE levels and immunologic measures in African–American farmers in North Carolina. Environ. Health Perspect. 112, 1080–1084. Cox, S., Niskar, A.S., Narayan, K.M., Marcus, M., 2007. Prevalence of self-reported diabetes and exposure to organochlorine pesticides among Mexican Americans: hispanic health and nutrition examination survey, 1982–1984. Environ. Health Perspect. 115, 1747–1752.

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Please cite this article in press as: Mercado, L.A., et al. Serum concentrations of p,p0 -dichlorodiphenyltrichloroethane (p,p0 -DDE) in a sample of agricultural workers from Bolivia. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2012.12.023