Diet and organochlorine contaminants in women of reproductive age under 40 years old

Early Human Development 65 Suppl. (2001) S173 – S182 www.elsevier.com/locate/earlhumdev

Diet and organochlorine contaminants in women of reproductive age under 40 years old C. Campoya,*, F. Olea-Serranob, M. Jime´nezb, R. Baye´sa, F. Can˜abatec, M.J. Rosalesd, E. Blancaa, N. Oleae a

Department of Pediatrics, School of Medicine, University of Granada, Avda. de Madrid, 11, 18012 Granada, Spain b Department of Nutrition and Bromatology, School of Pharmacy, University of Granada, Spain c Pediatrics Service, Hospital de Poniente, ‘‘El Ejido’’, Almerı´a, Spain d Department of Statistics, School of Pharmacy, University of Granada, Spain e Department Radiology, School of Medicine, University of Granada, Spain

Abstract The diet of the breast-feeding mother impacts on the quality and quantity of the milk that she feeds her child. Milk can be a vehicle for toxins, such as drugs and their metabolites, viruses, nicotine, caffeine, alcohol, and organochlorine molecules such as PCBs, DDT, HCB, HCH and dioxins, which can harm the health of the breast-feeding child. The 24-h recall diet was considered appropriate to adequately study the diet of breast-feeding mothers and was used in the present preliminary study to establish the possible relationship between the food items consumed and the presence of pesticides in her milk. Two groups of randomly selected healthy breast-feeding volunteers aged between 17 and 35 years from two different areas were recruited: 34 from intensive agriculture zone, El Ejido (Almeria), from the ‘‘Hospital de Poniente’’ and 21 urban zone, the city of Granada, from the ‘‘Clinico’’ University Hospital. Application of the Spearman Correlation Test to the results from Almeria showed a certain positive correlation between the total intake of fats and both the p,p0DDD (r = 0.53, p  0.05) and methoxychlor (r = 0.48, p  0.05) in mature milk, and between the energy supplied by vegetables and the endosulfan-lactone in mature milk (r = 0.50, p  0.05). Among the group of breast-feeding women from Granada, there was a strong correlation between the intake of fats and both the p,p0DDT in transition milk (r = 0.90, p  0.05) and the p,p0DDD in mature milk (r = 0.90, p  0.05). In conclusion, there is a statistically significant relationship between the consumption of fatty foods and some organochlorine molecules and

*

Corresponding author. Tel./fax: +34-958-244051. E-mail address: [email protected] (C. Campoy).

0378-3782/01/$ – see front matter D 2001 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 3 7 8 - 3 7 8 2 ( 0 1 ) 0 0 2 2 0 - 1

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between the consumption of vegetables and pesticides, and the latter relationship occurs in Almeria but not in Granada. D 2001 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Diet; Breast-feeding mother; Organochlorine pesticides; Human milk

1. Introduction The health risk for humans and animals posed by exposure to residues of chemical products in foods has yet to be fully defined. Pesticide residues are commonly detected in foods and although the concentrations have decreased by more than half during the past two decades, the residues in daily consumed foods are close to or above the maximum limits established by the FAO/WHO [1,2]. Lipid-rich foods and fish are generally sources of exposure to PCBs and DDE in industrialised countries. The total consumption of meat provides the best prediction of concentrations of dieldrin and a-HCH and the total consumption of fish the best prediction of PCBs [3]. The identification and determination of p,p0DDE in the fatty tissue of postmenopausal women from five European cities was positively related to the frequent intake of fish. The consumption of fish by girls during infancy and adolescence is considered to increase their risk of giving birth to lower-weight babies if they become mothers [4,5]. Foods in common use contain organochlorine pesticides, among other contaminants, although mostly at levels below the maximum limits authorised for residues. Analyses carried out in Denmark showed that these limits were not exceeded in animal-derived products, fruit or other fresh vegetables [6]. An analysis of the 5000 most widely consumed foods in the USA showed that very few contributed in a major way to the intake of contaminants. Out of a total of 300 pesticides and related molecules, only 63 were detected with any frequency, among which the metabolites of DDT and endosulfan were the most common. Since 1983, the levels of total residues of HCH in different Japanese foods have fallen, whereas in Taiwan, despite the official prohibition of some organochlorine pesticides since 1974, foods have shown significant levels of dieldrin, endrin, DDE, DDT, heptachlor, a- and b-HCH and a-endosulfan [7,8]. There is increasing evidence of the world-wide nature of the problem. HCH, DDT, chlordane, aldrin, dieldrin and PCBs have been detected in samples of cereals, spices, edible vegetables, milk, butter, edible oils, fish and meat in developed countries in Asia and the South Pacific and in Mexico [9,10]. In Europe, animal meat is a source of these molecules, although they have not been found above the EU maximum limits [11,12]. However, in Australia, where the maximum limit for endosulfan is 0.2 mg/kg, some samples contain more than 0.36 mg/kg, which is almost four times the internationally recommended maximum limit. The refining of fish oil can reduce but not eliminate the concentrations of the most volatile organochlorine contaminants (HCB, lindane and aHCH). However, the presence of this oil in dietary supplements is not taken into account in estimations of the mean daily intake of these organochlorine contaminants [13,14]. Common commercial milks that undergo heat treatments still contain significant levels of organochlorine pesticides [15 – 21].

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Table 1 Macronutrients in the diet of the women studied mean daily intake: questionnaires evaluated: Almerı´a (Al), n = 306 and Granada (Gr) n = 189

Mean SD ± Maximum Minimum

Energy (kcal)

Proteins (g)

Lipids (g)

Carbohydrates (g)

Fibre (g)

Al

Gr

Al

Gr

Al

1856.52 301.87 2801.90 1358.65

1921.0 179.07 2305.00 1591.20

80.21 16.57 158.30 55.70

80.73 9.40 99.90 59.70

93.00 24.10 154.10 5.30

Gr

Al

Gr

Al

Gr

99.26 9.67 114.40 84.90

173.97 22.47 245.70 135.30

189.70 22.82 236.30 148.40

9.37 2.34 14.20 6.10

10.41 2.38 16.10 5.20

It is clear that the diet of the breast-feeding mother impacts on the quality and quantity of the milk that she feeds her child, although it has little influence on its protein or mineral content. If the mother’s diet lacks certain vitamins, her milk will also be low in these vitamins [22,23]. There is also evidence that breast-feeding children are exposed to contaminants via the placenta and continue to be exposed through the milk they receive from their mother [24 – 27]. Milk can be a vehicle for toxins, such as drugs and their metabolites, viruses, nicotine, caffeine, alcohol, and organochlorine molecules such as PCBs, DDT, HCB, HCH and dioxins, which can harm the health of the breast-feeding child [28 –33]. The concentration of pesticides increases as they rise up the food-chain, so that human milk contains higher concentrations of pesticides than does cow’s milk. As a general rule, carnivores store more DDT than do herbivores [34,35]. In the 1960s, the concentrations of DDT in human milk exceeded 50 mg/l [36 –38] and in the 1970s, these concentrations remained at almost the same levels, although below the limits established for cow’s milk [39,40]. Currently, because of the persistence of organochlorine molecules and the continuing utilisation of many of these products, their presence in human milk remains extremely common. Evidently, the diet will influence the concentrations of pesticides stored in the human organism. Knowledge of the dietary habits and food consumption of a population is provided by dietary surveys. The aim of this preliminary study was to recopile 24-h recall diet was considered appropriate, to adequately study the diet of breast-feeding mothers, and was used to establish the possible relationship between the food items consumed and the presence of pesticides in her milk. In parallel with the research described in this paper, our group also determined the organochlorine pesticides present in the milk of the same women [41].

Table 2 Distribution of fatty acids in the diet PFA %

Mean SD ± Maximum Minimum

MFA %

SFA %

Cholesterol (mg)

Al

Gr

Al

Gr

Al

Gr

Al

Gr

9.47 3.79 29.20 7.00

9.76 5.11 31.50 6.90

52.46 4.45 68.70 43.70

52.09 3.06 56.00 41.50

40.25 6.51 70.50 29.00

39.59 4.63 57.50 34.80

66.66 17.41 95.90 23.40

71.37 30.26 183.90 20.70

PFA: polyunsaturated fatty acids, MFA: monounsaturated fatty acids, SFA: saturated fatty acids.

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Ca (mg)

Mean SD ± Max Minimum

Vit. B2 (mg)

Niacin (mg)

Vit. A (mg)

Vit. D (ug)

Vit. C (mg)

Al

Gr

Al

Gr

Al

Gr

Al

Gr

Al

Gr

Al

Gr

Al

Gr

885.13 259.24 1453.3 281.0

869.24 128.14 1167.1 566.2

7.93 1.32 11.70 5.50

8.04 1.20 11.0 6.30

1.50 0.35 2.30 0.60

1.55 0.23 2.00 1.10

25.12 6.30 55.40 19.0

25.42 3.60 34.10 19.70

687.76 277.04 1934.3 375.20

671.40 164.70 1075.9 492.70

2.39 2.10 10.50 0.60

2.54 1.90 9.20 1.10

83.80 48.74 281.3 31.50

91.89 54.22 277.4 35.70

Al: Almeria; Gr: Granada.

Fe (mg)

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Table 3 Micronutrients in the diet of the women studied

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At the Widespread II environmental conference, the working session on environmentally induced alterations in development drew the following conclusions: (1) there must be a reduction in the exposure of animals and plants to chemicals used by humans, (2) human beings and wild animals have exceeded their capacity to compensate for their exposure to these substances, (3) the exposure – risk relationship needs to be estimated. There are many gaps in our knowledge of this issue, and legislation is required to regulate and provide correct information on the health risks [42]. Programmes to monitor human milk have been put in place in several countries to establish the extent and significance of human exposure to organochlorine compounds. The food habits and occupation of the mother are very important in this context, and it has been suggested that there must be evaluation of qualitative and quantitative exposure from contaminating industries.

2. Material and methods We recruited two groups of randomly selected healthy breast-feeding volunteers aged between 17 and 35 years from two different areas: (a) intensive agriculture zone, El Ejido (Almeria), from the ‘‘Hospital de Poniente’’ (n = 34) and (b) urban zone, the city of Granada, from the ‘‘Clinico’’ University Hospital (n = 21). A total of 306 questionnaires were administered in Almeria and 189 in Granada. The study was approved by the Ethics Committees of the institutions that hosted the study. The questionnaires were administered three times during each of three distinct periods of lactancy, so that every woman in the study completed nine questionnaires. The periods were: during the first 3 days postdelivery, between 5 and 15 days post-delivery, and finally between 15 and 30 days postdelivery. If the size of any portion was missing from a completed questionnaire, the standard values for the Spanish population were used [43 –45]. A total of 495 dietary 24-h recall questionnaires were analysed, using a computer package based on a programme that manages a database containing the Wander food Table 4 One-way ANOVA results for Almeria and Granada Nutrients

F

p

Energy (kcal) Protein (g) Lipids (g) Carbohydrate (g) Fibre (g) Cholesterol (g) Ca (mg) Fe (mg) Vit. B2 (mg) Niacin (mg) Vit. C (mg) Vit. A (mg) Vit. D (mg)

0.78 0.17 1.28 6.29 2.55 0.54 0.07 0.11 0.42 0.04 0.33 0.06 0.08

0.38 0.90 0.26 0.02 0.12 0.47 0.80 0.75 0.52 0.85 0.57 0.81 0.78

Total degrees of freedom (df ) = 54; Inter-group df = 1; Intra-group df = 53.

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Table 5 Goodness of fit

Energy (kcal) Proteins (g) Lipids (g) Carbohydrates (g) Fibre (g) Vit. B2 (mg) Niacin (mg) Vit. A (mg) Vit. D (mg) Vit. C (mg) Ca (mg) Fe (mg)

Z of Kolmogorov – Smirnov

p

Al

Gr

Al

Gr

0.674 0.897 1.030 0.757 0.513 0.865 1.588 1.167 1.435 0.988 0.549 0.620

0.644 0.879 0.677 0.469 0.705 0.609 0.513 0.693 1.096 0.824 0.619 0.988

0.754 0.397 0.239 0.615 .955 0.443 0.013 0.131 0.032 0.283 0.924 0.836

0.801 0.422 0.749 0.981 0.704 0.853 0.955 0.723 0.181 0.506 0.838 0.284

composition tables, including the Spanish composition tables [46]. The SPSS 9.0 statistical programme for Windows was used to relate the nutrients supplied by the diet to the content of organochlorine pesticides in the human milk of these women. These data on the organochlorine pesticide content and the methodology utilised are presented in the associated study in this issue [41].

3. Results The results of the nutritional evaluation were divided between those from the rural (Almeria) and those from the urban (Granada) populations. The most important macronutrients and micronutrients were studied (Tables 1, 2 and 3). An inferential Table 6 Comparison of means of Al (df = 33) and Gr (df = 20) with RDA p Nutrients

RDA

Energy (kcal) 2700 Protein (g) 65 Lipids (g) 160 Carbohydrates (g) 250 Ca (mg) 1200 Fe (mg) 15 Vit. B2 (mg) 1.8 Niacin (mg) 20 Vit. C (mg) 95 Vit. A (mg) 1300 Vit. D (mg) 10

Al

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.190 0.000 0.000

Gr

Difference of means

Confidence interval for the difference

Al

Lower

0.000  779.0 0.000 15.7 0.000  60.7 0.000  60.3 0.000  330.8 0.000 6.9 0.000  0.2 0.000 5.4 0.796  3.1 0.000  628.6 0.000  7.5

Gr

 843.5 15.2  67.0  76.0  314.9  7.1  0.3 5.1  11.2  612.2  7.6

Upper

Al

Gr

Al

Gr

 860.5 11.5  65.1  70.7  389.1  7.5  0.4 3.8  27.8  703.6  8.3

 948.8 9.4  75.4  83.9  405  7.6  0.5 2.9  28.2  708.9  8.4

 698 20.0  56.3  49.9  272  6.4  0.1 7.1 21.6  553.6  6.6

 738.2 21.0  58.6  68.2  224.4  6.6  0.2 7.3 5.8  515.6  6.9

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Table 7 Relationship between the mother’s diet and the presence of organochlorine pesticides in human milk (Spearman’s correlation analysis) Almerı´a

Granada

Mature milk 0

Ingesta de grasa/p,p DDD Ingesta de grasa/p,p0DDT Ingesta de grasa/metoxicloro Energı´a vegetales/endo-lactona

Mature milk

Transition milk

r

p



p

r

p

0.529 – 0.479 0.459

0.024 – 0.044 0.035

– 0.900 – –

– 0.037 – –

– 0.900 – –

– 0.037 – –

statistical analysis was performed to determine any statistically significant differences according to the origin of the woman (Granada vs. Almeria) or in the mean intake of macro- and micronutrients. The distribution in the samples was analysed using the Kolmogorov –Smirnov test for one sample (Table 4). The one-way ANOVA test was used to compare the intake of nutrients between the two groups (Table 5). The Student’s t-test was used to compare the mean intake of nutrients in the different populations with the Recommended Dietary Allowances (RDA) [47] (Table 6). When data were not normally distributed, the Spearman correlation coefficient test was applied to contrast the possible degree of association between nutrients and pesticides content of the milk (Table 7).

4. Discussion The breast-feeding mother is continually exposed to small doses of toxins in her daily diet, as she has been throughout her life. To estimate this exposure it is necessary to determine the total daily intake. Only four or five 24-h recall questionnaires need to be applied to obtain reliable data on most of the nutrients, including some micronutrients (vitamins A and D, Niacin) and minerals (Fe or Ca) [48]. Little is known about the effects that might be produced by the continual intake of contaminated foods [49,50]. The present survey results showed no differences in the mean daily intake of energy between the two groups of women. None of the women from Granada and only 2% of the women from Almeria received the RDA-recommended energy intake. With respect to the mean daily intake of macronutrients (Table 5), there were differences in the intake of carbohydrates between the women from Granada and those from Almeria ( F = 6.29; p = 0.02). None of the women received the recommended intake of carbohydrates and only 2.9% had the recommended lipids intake, whereas the protein intake of 80.5% of the women was above the RDA recommendations. The differences between the means and the RDA recommendations were greater in Granada than in Almeria for lipids and carbohydrates, whereas the differences for proteins were similar (Table 6). Regarding the mean daily intake of micronutrients, all of the women received more than the RDA values for niacin, whereas none of them reached the recommended levels of Fe. Adequate calcium was consumed by 14.7% of the women

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from Almeria and only 9.5% of those from Granada. Adequate vitamin C was consumed by 2.9% of those from Almeria and 14.3% of those from Granada (Table 6). To summarise, the present survey shows that the intake of some nutrients by these populations of women does not meet the 1989 RDA recommendations. There is an excessive consumption of proteins and a deficient supply of carbohydrates and lipids. Their intake of lipids is very different from that of the general population, among whom there tends to be an excessive consumption of fats. Through the action of the food chain, highly persistent organochlorine molecules are found in the milk of mammals [4,18,21,51,52]. Eighty-five percent of the women from Granada consumed fish compared with only 41.7% of those from Almeria. However, no relationship was found between fish consumption and pesticide levels in the milk of these women. Application of the Spearman Correlation Test to the results from Almeria showed a certain positive correlation between the total intake of fats and both the p,p0DDD (r = 0.53, p  0.05) and methoxychlor (r = 0.48, p  0.05) in mature milk, and between the energy supplied by vegetables and the endosulfan-lactone in mature milk (r = 0.50, p  0.05). Among the group of breast-feeding women from Granada, there was a strong correlation between the intake of fats and both the p,p0DDT in transition milk (r = 0.90, p  0.05) and the p,p0DDD in mature milk (r = 0.90, p  0.05). In conclusion, there is a statistically significant relationship between the consumption of fatty foods and some organochlorine molecules and between the consumption of vegetables and the presence of pesticides in human milk, and the latter relationship occurs in Almeria not in Granada. Acknowledgements We thank Richard Davies for editorial assistant. This research was supported by grant from the EU Commission QLRT-1999-01422.

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