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Malaria control and levels of DDT in serum of two populations in KwaZulu H. Bouwman Ngxongo

a e

b

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, R. M. Cooppan , P. J. Becker & S.

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Research Institute for Environmental Diseases , Medical Research Council , Pretoria, Republic of South Africa b

Research Institute for Diseases in a Tropical Environment , Medical Research Council , Durban, Republic of South Africa c

Institute for Biostatistics , Medical Research Council , Pretoria, Republic of South Africa d

KwaZulu Department of Health , KwaZulu Government , Jozini, Republic of South Africa e

Dept. of Zoology , Potchefstroom University , for CHE, Potchefstroom, 2520, Republic of South Africa Published online: 19 Oct 2009.

To cite this article: H. Bouwman , R. M. Cooppan , P. J. Becker & S. Ngxongo (1991) Malaria control and levels of DDT in serum of two populations in KwaZulu, Journal of Toxicology and Environmental Health: Current Issues, 33:2, 141-155, DOI: 10.1080/15287399109531514 To link to this article: http://dx.doi.org/10.1080/15287399109531514

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MALARIA CONTROL AND LEVELS OF DDT IN SERUM OF TWO POPULATIONS IN KWAZULU H. Bouwman Research Institute for Environmental Diseases of the Medical Research Council, Pretoria, Republic of South Africa

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R. M. Cooppan Research Institute for Diseases in a Tropical Environment of the Medical Research Council, Durban, Republic of South Africa P. J. Becker Institute for Biostatistics of the Medical Research Council, Pretoria, Republic of South Africa S. Ngxongo KwaZulu Department of Health, KwaZulu Government, Jozini, Republic of South Africa

Concentrations of p,p'-DDT, p,p'-DDE, and p,p'-DDD were determined in serum of members of households of two different areas of KwaZulu. Annual intradomiciliary application of DDT is used for the interruption of malaria transmission in one area (the exposed group) while the other served as the control. Demographic differences between the two groups resulted in significantly more females in the control group. The two groups were comparable with respect to age. Serum from household members living in DDT-treated dwellings had significantly higher (p < .005) levels of ΣDDT and metabolites (mean ΣDDT 140.9 μg/l) than those from the control area (mean ΣDDT 6.04 μg/l). Percentage DDT was also significantly higher (p < .05) in the exposed group (28.9%) than the control group (8.3%). ΣDDT for

Prof. C. H. J. Schutte of the MRC is thanked for his assistance and encouragement. The KwaZulu Department of Health (in particular Dr. G. M. Short) and the South African Department of Health and Population Development (Mr. M. J. Botha) are thanked for their invaluable assistance. Mrs. J. Nkomokazi, Mr. C. Ngcobo, and Mr. Ndlazi, and his team are thanked for their excellent technical assistance. Mrs. B. Bouwman is thanked for her assistance with the preparation of this document. This work was supported by the Medical Research Council and published with their permission. Requests for reprints should be sent to H. Bouwman, at his present address, Dept. of Zoology, Potchefstroom University for CHE, Potchefstroom, 2520, Republic of South Africa. 141 Journal of Toxicology and Environmental Health, 33:141-155, 1991 Copyright © 1991 by Hemisphere Publishing Corporation

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the 3-10 yr age interval (168.6 μg/l) was significantly higher (p < .05) than the 20-29 (60.5 μg/l) and 30-39 (84.2 μg/l) yr age intervals. There seemed to be two groups with regard to accumulation and elimination. The age group 3-29 appeared to be eliminating DDT, most likely accumulated from contaminated breast milk, faster than they accumulated it. From around 29 yr of age accumulation predominated as the levels increased with age. Regression analysis suggested pharmacokinetic differences for DDE and DDT between the two groups. Liver function parameters between the two groups only differed significantly for gamma-glutamyl transferase (γGT) (p < .005), but the influence of difference in alcohol consumption, which was significantly higher in the exposed group (p < .0001), offered a better explanation. Those of the exposed group that consumed alcohol had a significantly higher (p < .05) mean γGT level (41.5 IU/I) than those that did not (20.2 IU/I), but were not significantly different for ΣDDT (p > .05). The safety of DDT used in malaria control for subjects aged 3 and older was confirmed by the levels of DDT in serum when compared with other studies, which showed lack of any negative effects associated with these levels in adults, and an apparently normal liver function in the exposed and control groups.

INTRODUCTION Serum levels of DDT and its metabolites can be used to determine body burden (Davies et al., 1969; Radomski et al., 1971; Brown and Chow, 1975). However, few studies have established the levels of DDT in the sera of populations protected by this insecticide against malaria. In areas where the mosquito vectors of malaria have not yet developed resistance to DDT, it remains the insecticide of choice. Large amounts are used in many parts of Africa and other tropical countries, protecting millions of people against malaria. The northern part of KwaZulu is one such area and has been protected since 1953 using focal sprays. Between 1957 and 1977 a 2-yearly comprehensive application of DDT was followed. Since 1977 DDT has been applied annually (from January to March) on the inner walls of the dwellings at 2 g/m2 (Sharp et al., 1988). During 1988, 98,912 dwellings, housing more than 300,000 people, were treated with 26,018 kg of 75% emulsifiable DDT (KwaZulu Department of Health, 1989). The lack of data on the levels of DDT in serum of the general population, especially for Africa, and the associated factors need to be addressed. The aim of this study was therefore (1) to determine the levels and composition of DDT in serum from an exposed population, (2) to determine the relationship between age and the levels as well as the composition of EDDT in an exposed population, and (3) to compare the levels and composition of EDDT and metabolites and liver function parameters with a group not exposed to DDT.

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MATERIALS AND METHODS

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Subjects

The study design and methods were approved by the Ethics Committee of the Research Institute for Diseases in a Tropical Environment. Serum samples were collected in the Ubombo (Northern Natal) and Port Shepstone (Southern Natal) districts during November 1986. Twelve households from the Mlambongwenya area in Ubombo, where DDT is used for malaria control, were selected as the exposed group (DDT has been banned for all other purposes since 1976; Van Dyk et al., 1982). A household was defined as all the members of the same family residing at a specific homestead. Length of residence (at least 10 yr) at the particular homestead was the criterion by which the households were selected by the Field Health Officer of Mlambongwenya (Mr. Ndlazi). Homesteads with cement structures were excluded (cement surfaces at the time of the study were treated with a 5% DDT emulsion). Permanent residence at the homestead was the criterion for recruitment of individuals (males and females) from the selected households. Informed consent, using Zulu as the spoken medium, was obtained from participants or their parents in the case of minors. This consent was obtained 2 wk before blood samples were taken, during which a comprehensive survey of the household was done. No blood samples were taken from children younger than 3 yr of age. Mlambongwenya is removed from major north-south migration routes, used by Mozambicans to obtain work in Natal and elsewhere. In a pilot study it was found that migrants from Mozambique, where hardly any malaria control is practiced, had very low levels of DDT, and this influenced statistical analysis (H. Bouwman, unpublished observations, 1987). Dwellings in Mlambongwenya are usually constructed of clay, branches, and thatch. Homesteads consist of 3-7 such structures and house from 4 to 22 people. The major source of income is from migrant labor in mines or farms. This labor is usually done by men between the ages of 20 and 40. These men, even if they were present temporarily, will not be exposed to DDT in the same way as permanent residents and were therefore excluded. The diet consists of staples such as maize and rice with meat from fish, goats, chickens, or cattle. This is supplemented by fruit, nuts, and roots collected locally. The control group was drawn from the Port Shepstone area (around the Murchison hospital) in Southern Natal where malaria does not occur. No DDT has been used there since 1976 (Van Dyk et al., 1982) for any purpose. The population from this area is stable, but more Westernized than the exposed population. Most dwellings were constructed from

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clay, but more cement structures were in evidence. Homesteads consist of two to four dwellings. Income was generated from labor in transport, plumbing, carpentry, and the tourist industry. Selection of individuals was done on the basis of length of local residence (in the "Muchasini" area as referred to by the local inhabitants) and no contact with potential sources of DDT (formulation of DDT, farming, and malaria control activities). The diet of the residents was essentially the same as for the Mlambongwenya population, but most of this was obtained from local retailers. There were no vegetarians nor smokers in this or the exposed group.

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Sample Collection

A questionnaire was completed for each participant. Information obtained included sex, age, previous residence, and occupational exposure to DDT or other pesticides. This was done in their own language, Zulu. Blood was collected by venipuncture. The blood was allowed to clot and serum was removed on the same day. Serum (2-ml samples) was stored in glass tubes and kept frozen. Another serum sample (-1.5 ml) was also frozen, and liver function enzymes and other parameters were determined by the Chemical Pathology Department of the King Edward VIII Hospital in Durban. Sample Preparation and Chromatography

Serum samples were extracted using a method previously described (Bouwman et al., 1989). Briefly, the serum was placed on a prewashed column consisting of 3 g of 1 : 1 mixture of silica gel and celite. The organochlorines were eluted with a dual solvent system. The extract was concentrated and analyzed using GC-ECD (gas chromatography with an electron-capture detector). The recoveries at different levels for different compounds ranged between 71 and 104%. The minimum detectable quantity was 0.5 pg per component. This method was developed to facilitate recovery of a fraction of the spiked compound that was not extracted after the spiked sample was frozen for longer than 24 h. Confirmation of peak identities was done by an independent laboratory using a different GC and column. Results presented here are not corrected for recovery. RESULTS

Subjects All members of all the households in the exposed group consented to participate. Some people from the control group, who agreed to participate a week earlier, refused when asked for a sample. Five households that were selected initially were therefore not sampled. Five other house-

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holds that fitted the criteria, from the same area, were recruited. Summary statistics of characteristics of the two groups are presented in Table 1. The frequencies of male and female for the two groups was tested using Fisher's exact test and found to be significantly different (p < .01). A Kolmogorov-Smirnov two-sample test was performed to determine whether the age variable from the two groups was drawn from the same distribution. The distributions were not significantly different (p = .247). A two-sided Student's f-test also revealed no significant difference between the mean ages (p = .288). Alcohol consumption was measured on a subjective, self-reporting scale of 1-4; 1 = no consumption, 2 = low, 3 = moderate, and 4 = high consumption. The exposed group averaged 2.65 for subjects 18 yr (n = 29) and older. For the control group it was 1.3 (n = 30). A two-sided Student's f-test of the log-transformed data showed that the two groups were significantly different (p < .0001) regarding the use of alcohol. This was confirmed by observations during visits. Serum Levels

All serum samples from the exposed group had detectable residues of DDT and DDE. Ten samples did not have detectable DDD. Of the serum samples from the control group, 71 were positive for DDE, 5 for DDT, and only 1 had detectable DDD. A Fisher's exact test for frequencies showed that these frequencies differed significantly between the exposed and control groups (p < .01). Cases where a particular parameter (e.g., DDE) fell below detection limit were treated as a missing value and not included in subsequent calculations for that parameter. The EDDT, DDT, DDE, and percentage DDT variables from the exposed group were log-normally distributed. Only the EDDT and DDE TABLE 1. Summary Statistics of Group Characteristics and DDT Levels in Serum from the Two Groups Parameter

Exposed

n Age Males Females DDE3 DDD a DDTa EDDTa

71 22.4 (18.4) 33 38 103.4° (85.1 )c [100]d 0.21° (0.7)c [14]d 37.3° (27.2)c [100]d 140.9° (108.3)c

a

Control

77 28.0 (23.0) 20 57

5.95 (7.98)c [92.2]d 0.015 (0.13)c [1.3]d 0.077 (0.31)c [6.5] d 6.04 (8.19)c

Units are /¿g/l (ppb). "Significantly different between groups (p < .05). Standard deviation. ^Percentage of the samples with levels exceeding the minimum detectable quantity.

H. BOUWMAN ET AL.

variables from the control group showed a log-normal distribution. DDD, DDT, and percentage DDT of the control group did not have enough values to allow for distribution determination. The age variable for both groups were log-normally distributed, and treated as such in all subsequent regression analysis and i-tests. A Kolmogorov-Smirnov two-sample test was performed to determine whether the EDDT and DDE variables from the two groups were drawn from the same distribution. They were significantly different (p < .0001). The results of the serum analysis are presented in Table 1. The differences (using two-sided i-tests) between the two groups were significantly different (p < .05). The relationship between DDT and DDE residues in serum from the exposed group was tested (Fig. 1). The multiplicative regression (V = aXb), which gave the best fit, was significant (p < .0001) with a coefficient of determination of 62.28%. The slope was 0.8866. This association, due to a lack of detected DDT, could not be tested in the control group. The age-related log-transformed EDDT-levels are presented in Figures 2 and 3. For the exposed group the analysis of variance indicated significant differences between age intervals. Two-sided i-tests (probing) were performed comparing levels between age intervals. For the exposed group, significance is proved by p values less than .00238 according to Bonferroni. A p value less than .05 indicates significant difference, but does not prove it. The 3-9 yr age interval was significantly different from the 20-29 and 30T39 yr age intervals. The differences between the 10-19 and 20-29 and between the 10-19 and 50-59 yr age intervals were possibly significant (p < .05). The 60-69 yr age interval of the control group 500 •

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DDT IN SERUM (u.q/1) FIGURE 1. Multiplicative regression of DDE on DDT in serum of the exposed group. The line represents the regression of the transformed data, while the dots represent the untransformed data.

DDE, DDD, AND DDT IN SERUM FROM KWAZULU

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Malaria control and levels of DDT in serum of two populations in Kwazulu.

Concentrations of p,p'-DDT, p,p'-DDE, and p,p'-DDD were determined in serum of members of households of two different areas of KwaZulu. Annual intrado...
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