Concentration of DDT compounds in breast milk from African women (Manhiça, Mozambique) at the early stages of domestic indoor spraying with this insecticide
Highlights
► DDT increases in pregnant women at the start of indoor spraying with this compound. ► Rapid transformation of DDT into DDE occurs in women after intake of this insecticide. ► The DDT increases in breast milk of women due to indoor spraying are not uniform. ► Breast milk DDT content in primiparae women is higher than in multiparae women. ► Women transfer a high proportion of their DDT and DDE body burden to their infants.
Introduction
Technical grade DDT is generally composed of 4,4′-DDT (∼80%), 2,4′-DDT (∼15%) and 4,4′-DDE (∼4%). This product started to be widely used as insecticide in the 40s, leading to the accumulation of 4,4′-DDT and its metabolites in many organisms due to their lipophilicity and high resistance to degradation. Humans are at the apex of the food chain and tend to bioaccumulate DDT compounds through diet, but in some cases direct exposure may also be a significant intake mechanism. DDT and its metabolites have also shown to generate adverse effects on the human health, such as on the cognitive development in children during their first years of life (Ribas-Fitó et al., 2006, Morales et al., 2008), alterations of thyroid hormone concentrations (Ouyang et al., 2005, Aneck-Hahn et al., 2007, Alvarez-Pedrerol et al., 2008a, Alvarez-Pedrerol et al., 2008b) or DNA damage (Yanez et al., 2004). Exposure to DDE, its main metabolite, has been related to increase of asthma incidence in infants (Sunyer et al., 2005, Sunyer et al., 2006) and increases in urinary coproporphyrins (Sunyer et al., 2008).
Evidence of the adverse effects of this insecticide in the environment and humans led to ban DDT for agricultural practices in the 1970s. Later, the Stockholm agreement led to a general ban of an important number of persistent organic pollutants, including DDT. These restrictions involved gradual reductions in DDT levels in large areas of the world, e.g. from breast milk contents of 5000–10,000 ng/g lipid in 1951 to ∼1000 ng/g lipid at present (Smith, 1999), or in Sweden between 2000 and 1300 ng/g lipid of 4,4′-DDE and 4,4′-DDT, respectively, to 130 and 14 ng/g lipid, respectively, in 1997 (Noren and Meironyte, 2000).
In Africa, where malaria killed 750,000 million people in 2009, insecticides have still been used to eliminate the malaria vector. The Stockholm Convention encouraged reducing reliance on DDT and promoting research and development on safer alternative pesticides and strategies. Many of these efforts have been concentrated on the use of pyrethroids as an alternative to combat the vector, which has been successful in some countries. However, the malaria mosquito has become resistant to pyrethroids (Hargreaves et al., 2003). Accordingly, more than two dozen countries, most of them from sub-Saharan Africa, requested exemptions on the ban of DDT for malaria vector control on the evidence that DDT was the most effective insecticide due to its persistence (it is sufficient to spray it just once a year in the houses), relatively low cost (about $5 per average five-person household) and efficiency. DDT either kills mosquitoes resting on the walls, or repels them from the dwellings (WHO, 2006, WHO, 2007).
The World Health Organization recommended the continued use of DDT in limited quantities for public health purposes in situations where alternatives were not available and where potential loss of human life associated with unstable malaria transmission and epidemics is greatest (WHO, 2006, WHO, 2007). One of the principal vector control interventions for reducing malaria transmission is indoor residual spraying (IRS). Reintroduction of DDT for IRS in some African countries like South Africa, Swaziland and Zimbabwe showed a rapid decline in the number of malaria cases in the areas treated with DDT (Mabasso et al., 2004, Maharaj et al., 2005).
DDT was introduced in 1946 in Mozambique where it was used widespreadly in agriculture and health programs until 1988. IRS programs with DDT were introduced in 1946 in the southern part. In 1950 all target areas were covered. As part of the malaria eradication initiative, IRS with DDT was carried out in the Maputo province between 1960 and 1969, but this program had a complete breakdown in the late 1970s due to the civil war (Mabasso et al., 2004). After the war, in 1993 there was a change in policy and the National Malaria Control Program (NMCP) decided to restart the IRS programs with pyrethroids (deltamethrin and lambda-cyhalothrin) in the major towns. In addition to this effort, the Lubombo Spatial Development Initiative (LSDI), an inter-country cross-border malaria control program (including IRS) jointly implemented by Mozambique, South Africa and Swaziland, commenced operations in southern Mozambique in 1999 (WHO, 2007). In 1999 initial baseline resistance to pyrethroids began to be detected in malaria vector mosquitoes (Casimiro et al., 2006a, Casimiro et al., 2006b, Sharp et al., 2006) which led to the implementation of changes from pyrethroids to carbamates (bendiocarb) in November 2000 as part of the LSDI (LSDI, 2006).
House spraying with DDT in Mozambique was introduced again at the end of 2005 in public health programs and has now become the main insecticide used for malaria vector control as no resistance to this product was detected in Mozambique (Casimiro et al., 2006a, Casimiro et al., 2006b, Casimiro et al., 2007, Cuamba et al., 2010). The houses and structures were sprayed once a year at an application rate of 3 g per m2. Currently the use of DDT in agriculture is still banned being restricted to mosquito control. To prevent illegal uses, DDT is exclusively distributed through the Ministry of Health (MISAU). However, misuses as consequence of poor management in rural areas cannot be excluded (MISAU, 2005, MISAU, 2006). Since 2005, MISAU has imported about 1300 tons of DDT (from India and China) in wettable powder which are still in use.
In other districts of the Maputo province (Matutuine, Namaacha, Boane, Moamba, Marracuene and Magude) spraying with DDT began between November 2005 and June 2006. In the Manhiça district, DDT was 45reintroduced for IRS in 2006 and was used together with bendiocarb. Between 2006 and 2008 there were three complete rounds of spraying. A global assessment of the benefits and drawbacks of the DDT reintroduction for malaria vector control is needed. Mozambique is a good case to study since this compound was banned for twelve years and then reintroduced with restrictions.
The past and present uses of DDT in Mozambique provide an example of the accumulation patterns of this compound and its metabolites at the early stages of reintroduction for public health policies. Breastfeeding is the primary source of early life infant nutrition. Infants are pre- and post-natally exposed to DDT compounds through the placenta and primarily breastfeeding. Due to the lipophilicity of DDT and its metabolites and the relatively high amount of fat in breast milk, it is common to find these compounds in human milk. Their concentrations in human milk may reflect the mothers’ body burden and can be used to estimate the dose transferred to infants. The IRS activities for malaria control can be a route for DDT uptake. Several reports have described significant concentrations of DDT in breast milk from women from African countries (Ejobi et al., 1996, Chikuni et al., 1997, Okonkwo et al., 1999, Sereda, 2005, Bouwman et al., 2006). However, no studies had previously been carried out to monitor the levels of organochlorine compounds (OCs) in Mozambique. The present study focuses on establishing the levels of DDT and its metabolites DDE and DDD in human milk in a rural area located south of the country. Samples were collected in 2002 (before IRS) and 2006 (after IRS reintroduction), therefore these two groups provide representative examples of DDT accumulation prior and at the early stages of IRS.
Section snippets
Study area
The Manhiça district is a rural area located in the north of the Maputo province, limiting with the Indian Ocean in the east. The climate is subtropical with two distinct seasons, one warm and rainy between November and April and another dry and cold from May to October. Most of the inhabitants are farmers who grow sugar cane, bananas and rice, and some of them work in two big sugar cane factories nearby.
The first round of IRS occurred between September 2006 and March 2007, using about 1600 kg
Participant profiles
Maternal age in the 2002 group ranged between 15 and 44 years, with mean and median of 26.1 and 25 years, respectively (Table 1). In the 2006 group, maternal age ranged between 15 and 47 years, with mean and median of 24.2 and 22 years, respectively (Table 1). In this last group there were 16 primiparae and 32 multiparae women (Table 3). These two groups showed significant age differences (p < 0.05; Table 3), the median differences being 6 years. The age of the oldest breastfed infant was 325 days.
DDT concentrations and in door residual spraying
The present study describes for the first time the DDT concentrations of breast milk samples in a rural population from Mozambique where DDT was reintroduced by IRS. Breast milk concentrations of OCs in 2006 were significantly higher than in 2002, the median of ∑DDT in 2006 being 2.9 times higher than in 2002. IRS with DDT is the main likely cause for the increase of this insecticide in maternal milk samples. These results are consistent with observations in other areas. Bouwman et al. (1990)
Conclusion
The use of DDT for IRS increased the general DDT breast milk concentrations of 4,4′-DDT and its main metabolite, 4,4′-DDE, in mothers from the Manhiça district already in the first stages of implementation of an IRS program. However, the observed median for 2006 is still low in comparison to breast milk concentrations in many world populations. The observed increases were not uniform and in some individuals the measured breast milk concentrations were high with respect to levels previously
Acknowledgements
We thank all the families for their participation in the study and the staff of the Manhiça Health Research Center for their support during data and sample collection. We thank M. Fort for her kind support with the lipid analysis of the samples collected in 2006. MNM is funded by a PhD Scholarship from Fundació Marfà. CD is supported by the Spanish Ministry of Science and Innovation (MICINN; RYC-2008-02631). The Centro de Investigaçao em Saúde da Manhiça receives core support from the Spanish
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