Elsevier

Environmental Pollution

Volume 144, Issue 3, December 2006, Pages 902-917
Environmental Pollution

Simultaneous presence of DDT and pyrethroid residues in human breast milk from a malaria endemic area in South Africa

https://doi.org/10.1016/j.envpol.2006.02.002Get rights and content

Abstract

DDT and pyrethroids were determined in 152 breast-milk samples from three towns in KwaZulu-Natal, South Africa, one of which had no need for DDT for malaria control. All compounds were found present in breast milk. Primiparae from one town had the highest mean ΣDDT whole milk levels (238.23 μg/l), and multiparae from the same town had the highest means for permethrin (14.51 μg/l), cyfluthrin (41.74 μg/l), cypermethrin (4.24 μg/l), deltamethrin (8.39 μg/l), and Σpyrethroid (31.5 μg/l), most likely derived from agriculture. The ADI for DDT was only exceeded by infants from one town, but the ADI for pyrethroids was not exceeded. Since the ADI for DDT was recently reduced from 20 to 10 μg/kg/bw, we suggest that this aspect be treated with concern. We therefore raise a concern based on toxicant interactions, due to the presence of four different pyrethroids and DDT. Breastfeeding however, remains safe under prevailing conditions.

Introduction

In both developing and developed countries, human breast milk remains the best sole nutrient source for infants (especially in the early stages of infancy), even though it could contain pollutants, such as PCBs and DDT (Sonawane, 1995, Pronczuk et al., 2004). The presence of DDT and other organochlorine compounds in human breast milk has been known for quite some time from malaria (Bouwman et al., 1992) and non-malaria areas (Savage et al., 1981). The restriction on or banning of many of these compounds for agriculture in most parts of the world has led to gradual reductions in the levels of organochlorine compounds in breast milk, especially in developed countries such as Canada and Sweden (Van Hove Holdrinet et al., 1977, Bernes, 1998, Shutz et al., 1998).

In Africa where malaria still kills more than a million people each year, the use of pesticides to interrupt the parasite transmission has continued to rely on insecticide treatment of dwellings, and insecticide treated bed nets (Kapp, 2004). The intention of international initiatives such as the Stockholm Convention and the Roll Back Malaria campaign is to reduce the reliance on DDT per se, and to use alternative methods, products and strategies. Much of the effort has concentrated on using synthetic pyrethroids as one such alternative, and some countries have successfully done so. One notable exception was the forced reintroduction of DDT in South Africa, after one of the mosquito vectors (that was previously eliminated from South Africa by DDT) returned, but with pyrethroid resistance (Hargreaves et al., 2000). The resulting increase in malaria cases and deaths was epidemic – malaria cases soared from 4117 cases in 1995 to 64,622 in 2000.

The Stockholm Convention (Anon, 2004), that was negotiated during this period in Johannesburg, South Africa, took note of this situation and a dedicated section on the conditions of use and production of DDT was negotiated, allowing countries to continue using DDT, but only with strong regulatory and reporting requirements (Anon, 2004). In order to move away from DDT, the Convention urges parties to promote research and development of safe alternative chemical and non-chemical products, methods and strategies relevant to the conditions of those countries, thereby reducing the human and economic burden of the disease. The alternatives, however, should also pose less risk to human health and the environment (Annex B, Part II). Parties are therefore allowed to continue using DDT, but alternatives should be investigated and implemented where possible. Some of the pyrethroids have been promoted, and in many places implemented as alternative indoor residual spray (IRS), or as treatment of bed nets (Goodman et al., 2001). These compounds are generally assumed safer to the environment, and at least benign to human health (Anon, 1998, Ray and Forshaw, 2000, Barlow et al., 2001, WHOPES, 2002). When switching from one chemical to another, and perhaps especially when moving away from DDT, it is inescapable that residues of the former will remain for an extended period (Bouwman et al., 1990a, Yanez et al, 2002). Just as DDT can be taken up by the inhabitants of treated dwellings (Bouwman et al., 1991), so too can humans be exposed to pyrethroids (or other compounds), and potentially excrete both via breast milk. We managed to trace only one published study that has found pyrethroids and organochlorines in the same human milk samples, and that was from Switzerland (malaria control was obviously not the source here) (Zehringer and Herrman, 2001). These authors have found nine pyrethroids (three others were not detected), as well as pyrethrins, in 53 breast-milk samples of mothers living close to Basle, Switzerland.

Malaria control is not the only potential source of human exposure to pesticides. Pyrethroids, organophosphates and carbamates, among others, have now taken over as major crop protection and veterinary chemicals. With increasing development in rural malaria areas, agriculture has changed from mainly subsistence, to a mixture of subsistence, cash crop and commercial farming. This, especially in the case of the northern areas of KwaZulu-Natal (Fig. 1), has meant that more insecticides are now being used. The same areas are still malaria endemic, and many of the homesteads are still subject to annual IRS. Therefore, inhabitants, many of whom are also active in agriculture, may be exposed outdoors in the fields, via food (including animal products) and water, as well as indoors to IRS (Bouwman, 1997). In addition, these compounds can wash into water bodies, and potentially give rise to resistant strains of vectors (Sereda and Meinhardt, 2003).

In developing countries, and especially in the rural areas of these countries, breastfeeding remains (and should be encouraged to remain) a primary source of food to infants. Previous studies done in KwaZulu-Natal, indicated that mothers breastfeed their infants for up to two years. This is a particularly long period, and it can lead to a significant transfer of pollutants to infants (Bouwman et al., 1992). It was found from this and other studies that primiparae mothers had higher concentrations of DDT in their milk (up to double the concentration) than multiparae mothers. The firstborns seem therefore to receive more pollutants via breast milk, when compared with their younger sibs.

This study will investigate the presence of and deliberate on the contribution from possible sources and routes of exposure of pyrethroids and DDT in breast milk of three semi-urban populations that experience various degrees of active malaria control and increased agricultural use of insecticides, some of which are pyrethroids. While previous studies in KwaZulu-Natal only analysed for p,p′-DDE, p,p′-DDT and p,p′-DDT, this study will also look at the o,p′ isomers, due its estrogenic activity (Bitman et al., 1968, Robison et al., 1985, Chen et al., 1997). We will also address some of the implications of these findings, including how it relates to the Stockholm Convention.

Section snippets

Study sites

We selected the Ubombo and Ngwavuma districts of the northern parts of the KwaZulu-Natal Province of South Africa. The region lies between Swaziland to the west, Mozambique to the north and the Indian Ocean to the east (Fig. 1). This area is well known due to intensive malaria, biodiversity and agricultural research, and is well characterised in terms of previous DDT investigations on humans and the environment in the 1980s and 1990s. Malaria transmission is endemic but normally low. Malaria

Participant profiles

A total of 152 mothers were successfully enrolled in this study. The number of mothers that successfully donated milk at each clinic is presented in Table 1, Table 2. Jozini, being the largest town in the region, had the highest number of participants, with smaller numbers attending the clinics at the other two towns. Ten mothers from Mkuze opted not to participate. All other mothers that were present at the other two clinics did participate. None of the mothers had any accidental or

Comparison with previous studies

Relevant to the objectives of this study, three major changes have taken place since the previous breast milk surveys done in 1987–88 (Bouwman et al., 1990b, Bouwman et al., 1990c, Bouwman et al., 1992); the much more extensive use of insecticides in agriculture, the interim period of pyrethroid use for malaria control, and the first year of resumption of DDT application (when the samples for this study were collected), following the failure of pyrethroids. The effects of all three of these

Conclusion

We need to realise that the situation described above is more or less experienced by millions of citizens in South Africa, and comparable numbers and conditions are also relevant in many other African countries. We have established the simultaneous presence of both DDT and pyrethroid residues in breast milk from a malaria-endemic area in KwaZulu-Natal, South Africa. The DDT levels were lower than previous studies, but the presence and levels of pyrethroids have added another level of

Acknowledgements

We would like to thank the Plant Protection Research Institute of the Agricultural Research Council for funding and conducting all physical research work as well as permission to publish, The National Research Foundation for funding, ARC-PPRI Pesticide Analytical Laboratory (Miss Marietjie Cloete, Mr Ephraim Malinga), KwaZulu-Natal Department of Health (particularly Mr Jotham Mthembu and Sakkie Hattingh), the personnel of the Mosvold and Bethesda hospitals, and the personnel of the Jozini,

References (51)

  • Anon

    The Stockholm Convention on Persistent Organic Pollutants

  • C. Bernes

    Persistent Organic Pollutants: A Swedish View of an International Problem, Monitor 16

    (1998)
  • J. Bitman et al.

    Estrogenic activity of o, p′-DDT in the mammalian uterus and avian oviduct

    Science

    (1968)
  • H. Bouwman

    Malaria, agriculture and health: Is there a connection?

    Plant Protection News

    (1997)
  • H. Bouwman et al.

    Environmental and health implications of DDT-contaminated fish from the Pongolo Flood Plain

    African Journal of Zoology

    (1990)
  • H. Bouwman et al.

    Levels of DDT and metabolites in breast milk from Kwa-Zulu mothers after DDT application for malaria control

    Bulletin of the World Health Organization

    (1990)
  • H. Bouwman et al.

    Factors affecting levels of DDT and metabolites in human breast milk from KwaZulu

    Journal of Toxicology and Environmental Health

    (1990)
  • H. Bouwman et al.

    Malaria control and levels of DDT in serum of two populations in KwaZulu

    Journal of Toxicology and Environmental Health

    (1991)
  • H. Bouwman et al.

    Transfer of DDT used in malaria control to infants via breast milk

    Bulletin of the World Health Organization

    (1992)
  • C.W. Chen et al.

    Transcriptional activation of the human estrogen receptor by DDT isomers and metabolites in yeast and MCF-7 cells

    Biochemical Pharmacology

    (1997)
  • O. Chikuni et al.

    Residues of organochlorine pesticides in human milk from mothers living in the greater Harare area of Zimbabwe

    Central African Journal of Medicine

    (1991)
  • F. Coulston

    Reconsideration of the dilemma of DDT for the establishment of an acceptable daily intake

    Regulatory Toxicology and Pharmacology

    (1985)
  • K. Czaja et al.

    Effect of age and number of deliveries on mean concentration of organochlorine compounds in human breast milk in Poland

    Bulletin of Environmental Contamination and Toxicology

    (1997)
  • G. Daston et al.

    A framework for assessing risks to children from exposure to environmental agents

    Environmental Health Perspectives

    (2004)
  • F. Ejobi et al.

    Organochlorine pesticide residues in mothers' milk in Uganda

    Bulletin of Environmental Contamination and Toxicology

    (1996)
  • Cited by (188)

    View all citing articles on Scopus
    View full text