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Research ArticleLinking Environmental Exposure with Public HealthDichlorodiphenyltrichloroethane Extracted from Soilsand Water of Recently Exposed Communities of SelectedLocations in Zambia
Nosiku Sipilanyambe Munyinda12 Charles Michelo1 and Kwenga Sichilongo2
1Department of Public Health Environmental Health Unit School of Medicine University of Zambia Zambia2Department of Chemistry Faculty of Science University of Botswana Gaborone Botswana
Correspondence should be addressed to Nosiku Sipilanyambe Munyinda ssikuhotmailcom
Received 16 May 2015 Revised 5 August 2015 Accepted 23 August 2015
Academic Editor Pam R Factor-Litvak
Copyright copy 2015 Nosiku Sipilanyambe Munyinda et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited
Background In 2000 a Zambian private mining company reintroduced the use of dichlorodiphenyltrichloroethane (DDT) tocontrol malaria in two districts From 2000 to 2010 DDT had been applied in homes without any studies conducted to ascertain itsfate in the environment We aimed to quantify the presence of DDT and its metabolites in the soil and water around communitieswhere it was recently used Methods We collected superficial soil and water samples from drinking sources of three study areasDDT was extracted by QuEChERS method and solid phase extraction for soils and water respectively Analysis was by gaschromatography-mass spectrometry A revalidated method with limits of detection ranging from 0034 to 004 ppb was usedResults Median levels of total DDT were found at 1004 (IQR 909ndash110) and 7254 ngL (IQR 540ndash7745) for soils and waterrespectively No DDT above detection limits was detected in the reference area These results are clinically significant given thepersistent characteristics of DDT Conclusion DDT presence in these media suggests possible limitations in the environmentalsafeguards during IRS Such occurrence could have potential effects on humans especially children hence there is a need to furtherexamine possible associations between this exposure and humans
1 Introduction
Present benefits versus discounted costsThis question is stillunanswered in terms of the use of DDT (dichlorodiphenyl-trichloroethane) a persistent organic pollutant used formalaria control inmany parts of Africa In Zambia malaria isstill the leading cause of morbidity and mortality accountingfor 36 of all hospital admissions with the majority beingpregnant women and children [1] In response to this highmalaria burden the government of Zambia through theMin-istry of Health developed an integrated vector management(IVM) strategy [1 2] This strategy focused on increasingcoverage of indoor residual spraying (IRS) activities inaddition to distribution of insecticide-treated nets (ITNs)expansion of environmentalmanagement and larviciding In2000 a privatemining company Konkola CopperMines was
the first to reintroduce DDT as one of its main chemicalsfor IRS after more than two decades since its use had beendiscontinued in Zambia [3] This followed the total ban ofDDT in the United States of America and other developedcountries in the early 1970s due to its negative environmentaleffects [4] These IRS activities were complemented by otherIVM interventions The apparent success of this programmein one mining town and the fact that IRS with DDT wasthe principal method by which malaria was eradicated orin some cases significantly reduced in many countries inthe world led the Zambian government in 2003 to initiateIRS activities initially in five pilot districts [1 5] SeveralWorld Health Organisation- (WHO-) endorsed insecticidesincluding DDT which was applied only to unplasteredsurfaces were used for this activity This initial coverage wasincreased to 15 districts in 2008
Hindawi Publishing CorporationJournal of Environmental and Public HealthVolume 2015 Article ID 564189 8 pageshttpdxdoiorg1011552015564189
2 Journal of Environmental and Public Health
Several studies have shown that DDT causes thinningof bird egg shells and finds its way into the food chain ifimproperly handled [6ndash8] It is an endocrine disruptor andhas been shown to cause other human health effects rangingfrom reproductive failure to increased incidences of differentcancers [4 9ndash25] Its main action is through the disruptionof the neurological functions of the brain by disturbingneurotransmitters mimicking Th4 a thyroid hormone anddisturbing the internal signalling system of synapses [21 25ndash35]
Locally 239758 kg of DDT has been used in Zambiasince 2000 with no documented studies being conducted onenvironmental and human exposures [36] Previous studieson DDT exposure in other settings involved historicallyexposed communities and looked mainly at its metabolitesDDE andDDDThe few studies done in South Africa focusedon reproductive outcomes in occupationally exposed malesand some in women [9 15] Given the potential harm thatDDT has been shown to cause in various locations aroundthe world coupled with the HIV pandemic and povertysituation in Zambia it is highly likely that these effects willbe more pronounced in the Zambian population So farno study has been carried out to ascertain the fate of therecently applied DDT in both the environment and humanhealth
To this effect we aimed to carry out an exposureassessment in selected areas of Zambia in order to quantifythe prevalence of DDT and its metabolites in soil andwater around communities where it was recently used Thiswork is part of a broader research project which aims tolink recent DDT exposure to neurodevelopmental outcomesin children of the targeted populations and also evaluateother factors that may be associated with the observedoutcomes
2 Materials and Methods
21 Study Areas The study areas comprised ChawamaChongwe and Mongu selected based on history of pastexposure to DDT in the last three years Chawama wasrandomly selected for this study as it was one of the pilot areaswhere DDT was applied in 2004 and has a very high malariaburden compared to the rest of Lusaka It is a periurban areain the center of Lusaka situated at 1535∘ south latitude 287∘east longitude and 1069meters above the sea level Chongweon the other hand is a rural town east of Lusaka situated at1535∘ south latitude 287∘ east longitude and 1069 metersabove the sea level It was also randomly selected amongamong two other areas Kafue and Mumbwa which are ruraldistricts within a 200 km radius to Lusaka as it was one ofthe areas where DDT was applied commencing in 2008 Incontrast Mongu is a town with a mixed urban and ruralpopulation located west of Lusaka situated at 1525∘ southlatitude 2313∘ east longitude and 1018 meters above the sealevel It was conveniently selected as the control area becausethere is no report of DDT application as part of governmentIRS activities [37] Mongu was selected as the reference areawhile Chawama and Chongwe are the areas where DDT wasapplied
Figure 1 Soil sampling pattern
22 Sampling The sampling for soil andwater in all the studyareas was done during July 2012 Compound samples werecollected from locations in the immediate periphery of thehouses
The inclusion criterion for the areas with recent applica-tion was that the residences should have been sprayed at leastthree times with DDT in the last 10 years
221 Soil A total of 14 soil samples were collected inChongwe (3) Chawama (7) and Mongu (4) In order to dis-cern recent exposure characteristics samples were obtainedfrom the top soil at a depth of 2ndash5 cm using bucket andtube augers depending on the type of soil present in thearea At each sampling point 500 g of the soil sample wascollected and placed in a nontransparent paper bag whichwas put into a plastic bag to avoid leakage In order to ensurerepresentativeness of the soil samples in the study areas azigzag sampling pattern was employed covering the entiresampling area in each community as illustrated in Figure 1
222 Water A total of 14 water samples were collected inChongwe (3) Chawama (7) and Mongu (4) respectivelyThe samples were obtained from various drinking watersources such as shallow wells open streams and communaltaps These samples were obtained using 1-litre water samplebottles which had been triple-rinsed with wash grade ace-tonehexane mixture The bottles had tightly fitted caps andlids to avoid spillages and enough space was allowed at theneck of the bottle to facilitate air exchange
The samples were transported to the Mass SpectrometryUnit in the Department of Chemistry at the University ofBotswana under the United Nations Transport of DangerousGoods (UNTDG) Regulations of 2011 [38] where they werekept in a cold room at sim4∘C until they were extracted andanalysed
23 Sample Extraction and Chemical Analysis231 Soil Samples A slightly modified AOAC Method200701 adapted by Nagel [39 40] using QuEChERS kitswas used for extraction of DDT from soil samples Twenty(20) grams of soil was weighed into a centrifuge tube and12mL of water was added and shaken for 4 hours afterwhich 20mL of acetonitrile was added for homogenization
Journal of Environmental and Public Health 3
The supernatant was thereafter quantitatively transferredto a second centrifuge tube containing 6 g MgSO
4 15 g
NaCl 15 g Na3Citrate dihydrate and 750mg Na
2HCitrate
sesquihydrate Centrifugation was done for 2 minutes at4500 rpm Sample cleanup was achieved by using dispersivesolid phase extraction using cartridges that contained 150mgprimary secondary amine (PSA) 400mg C18EC and 900mgmagnesium sulfate of between 985 and 1015 purity In eachextraction 6mL of supernatant was transferred into an SPEcartridge and shaken for 1 minute before centrifugation for2 minutes at 4500 rpm The organic layer was filtered usinga syringe and a membrane filter (045mm) and then evapo-rated under nitrogen to 1mLThe concentratewas transferredinto a 2mLGC vial and was ready for gas chromatography-mass spectrometry (GC-MS) analysis
232 Water Samples The standard solid phase extraction(SPE) method of conditioning loading washing and elutionwas used for the extraction of DDT from the water samplesThis was achieved using Florisil SPE Cartridges and anAgilent vacuum manifold (VacElut SPS 24) The procedurewas a slight modification of a method developed in thelaboratory for the determination of PCBs in transformer oil[41] Eight (8)millilitres of hexanewas added to condition thecartridge followed by 8mL of deionised water at 1mLminThis was followed by loading 20mL of the water sample at aflow rate of 05mLminThe cartridge was allowed to dry foranother 20 minutes to allow for interaction of the DDT withthe stationary phase
Five (5) millilitres of hexane was eluted through thecartridge to wash off any nonpolar analytes that couldhave bound strongly to the stationary phase Elution ofthe DDT was accomplished by running 10mL of a 5 5 n-hexane acetone mixture The resulting eluate was blowngently under a stream of nitrogen to concentrate it to 05mLand transferred to GC vial for GC-MS analysis
24 GC-MS Conditions An Agilent (Palo Alto CA USA)5975 C series gas chromatograph-quadrupole mass spec-trometer (GC-qMS) system equipped with a selective massdetector was used for analysis The system has capability toperform ion manipulation in the full scan and selected ionmonitoring (SIM) modes It also has two ionization modesthat is electron ionization (EI) and chemical ionization (CI)In this study the SIMmode was used after CI using methaneas a reagent gas Helium was used throughout as a carriergas at a flow rate of 1mLmin The oven program for the GCwas as follows The column was held at 80∘C for 2min andthen ramped at 10∘Cmin up to 270∘C for a total run timeof approximately 30 minutes The injector was held at 270∘CThemass spectrometer was operated in the negative chemicalionization (NCI) mode for soil analysis while the electronionization (EI) mode was used for water sample extractsAll the instrumental settings used were optimized prior toapplication on real sample extracts The Automated MassSpectral Deconvolution and Identification System (AMDIS)by the National Institute for Standards and Technology(NIST) in conjunctionwithMicrosoft Excel was used for data
analysis Extraction efficiencies were determined by analysisof spiked sample extracts with the analytes of interest
25 Quality Control For quality control and assurance pro-cedural blanks were extracted with n-hexane and subjectedto the same extraction procedure as the other samples Thesewere run with every ten samples in addition to field andlaboratory blanks Descriptive statistics were used to describedata and the term tDDT was used to refer to the sum of allDDT and its metabolites DDE and DDD In the presentationof the results however a distinction was made as to whichDDT metabolite was being referred to
26 Ethics Written permits were acquired from theMinistryof Mines andMineral Resources to export the soils and waterinto Botswana for analysis The Botswana Unified RevenueService also gave entry permission for the samples
3 Results
31 DDT Distribution and Validation A summary of vali-dation results derived from 6 point calibration curves withcorresponding regression equations is presented in Table 1
From Table 1 reasonably good extraction efficiencieswere attained using both QuEChERS and SPE extractionsLow detection limits were also estimated in both soil andwater samples and when these are compared to the 1120583gLwhich is the World Health Organization (WHO) MaximumRecommended Limit (MRL) for DDT and its derivatives indrinkingwater theywere found to be low enough for analysis
Results of concentrations of DDT and its metabolites inthe study areas are summarized in Figure 2
Figure 2 shows that all analyteswere present in all the soilsof Chawama and Chongwe However they were all foundto be below the LoDs in Mongu which was our referencearea The concentrations varied in all the study areas butthe highest amounts of DDT at 258 ngg were determinedaround a rural homestead of Chongwe followed by 257 nggin soils collected very close to the exterior walls of a house inChawama Township DDT accounted for 12 of the tDDT inthe soils sampled In some areas the percentage was as highas 27
Inwater the sample analysis results are shown in Figure 3DDT in water was found in 6 out of the 14 sampling
points No DDT above the limits of detection was detectedin water samples fromMongu which was the reference sam-pling site In general the lowest amount of DDT accountedfor 4of the tDDTwhile the highest concentration at 511 nggwas detected around a pit latrine in Chawama Townshiptranslating into 75 of tDDT
4 Discussion
DDT levels were found in significant levels in both water andsoils in the study areas of Zambia These high levels weremost prominent in sites with a history of DDT exposurethrough the IRS program for malaria control No DDTabove the limits of detection was found in the reference
Figure 2 DDTDDE andDDDconcentrations in soil samples fromChawama and Chongwe
0200400600800
10001200
DDT DDE DDD tDDTMetabolite
DDT concentrations in water by location
Chawama blue water ChawamaChawama-Kuku Chawama-Ngwenya DamChongwe-Mulilanduba Chongwe-Choombwa
Con
c (120583
gL)
Figure 3 DDT DDE and DDD concentrations in water samplesfrom Chawama and Chongwe
area In soil from the two Zambian study areas the medianconcentrations were twice or higher than those reported inSpain Uganda and South Africa among selected countrieswhere they were 46 59 and 43 ngg respectively [42ndash44]
It is possible that there might be inherent samplingerrors and that coincidentally both sampled sites with recentexposure could have higher DDT concentrations as foundin this study However given that every effort was made torandomly select the locations and sampling sites it is unlikelythat these sampling errors could be important enough toexplain these resultsWe therefore reasonably argue that whatwas found in this exposure assessment could be from recentexposure
DDT has not been sprayed in Zambia since 2010 whenevidence of mosquito resistance to it began to emerge [45]DDT and its metabolites can persist in soil for 2ndash15 years [8]and therefore the period of recent exposure still falls withinthe half-life brackets for DDT The soil sampling protocolrestricted the depth at which the soil samples were collectedto the A and E horizons which are generally about 06ndash45m
below the surface and typically lose minerals and chemicalsdue to leaching over time [46] The study conducted inKenya by Lalah et al showed that DDT and other pesticidesmetabolize faster at varying rates depending on the soil typedue to environmental factors such as prevailing climaticconditions pH of the soil and the action of microorganismsIt has been shown to degrade even faster in temperateclimates such as the one found in Zambia
DDT has a much longer half-life of up to 150 years inwater and due to its lipophilic nature it tends to gravitatetowards organic material and other such fatty tissues Its veryhigh concentrations in the water bodies where the sampleswere collected were a surprising and alarming result Themedian concentrations of DDT were found to be more thantwo hundred times higher than those recorded inNigeria andSouth Africa at less than 0368 and 2120583gL respectively Thisis against the background in which the WHO has recom-mended a maximum of 1120583gL per 001mgkg of body weightcalculated at the assumption that a 10 kg child drinks up to 1litre per day [47]These results corroborate the findings fromthe 2010 Environmental Council of Zambia (ECZ) audit ofIRS activities which showed lapses in the implementation ofenvironmental safeguards during the spraying exercises [36]
No DDT and its metabolites above detectable limits weredetected in the reference area in both soil and water samplesMongu was not included in the IRS program due to itsproximity to the Zambezi River a source of livelihood andnutrition for the local communities Despite the historicalapplication of DDT in the 1940s to the 1980s for otherpurposes in Mongu the sampling of only elluvium A top soilcould havemasked residues whichmost likelymay be presentin the lower strata Given the rapid velocity of the water in theZambezi River and the high water table inMongu it is highlyunlikely thatDDT could have remained in the aquatic systemThis coupled with the presence of many aquatic species andother organic materials in the water bodies in this area couldhave resulted in the DDT sequestering itself in them due toits lipophilicity
These results are clinically significant given the bioaccu-mulation and biomagnification characteristics of DDT as ittravels up the food chain [7 8 47 48] Several studies invarious settings of the world have shown that DDT in plantsis taken up through the roots and when these plants areconsumed by both humans and animals the DDT remainssequestered in these speciesrsquo adipose tissue This is also truewhen DDT sequesters itself in aquatic species which areedible to humans and animals These studies also show thatthe primary exposure route for humans to DDT is throughingestion of contaminated foods and water [47]
The high tDDT concentrations found in the studysites and subsequent DDT contamination burden may bean indication of challenges associated with environmentalmonitoring of such pollutants especially in resource poorsettings already plagued with high malaria incidences amongother public health challenges (Table 2) Given that thesehighly exposed areas are also often inhabited by very poorpopulations most of whom are women and children thisposes an ethical dilemma to decision makers on the cost-effectiveness of reintroducing DDT Speculations were raised
6 Journal of Environmental and Public Health
Table 2 Summary description of tDDT concentrations inChawama and Chongwe
by several scholars on the effectiveness of the reintroductionof DDT formalaria controlThe researchers in [10 49 50] arethus justified This is based on results of studies such as thisone and that conducted in South Africa also which showedthat DDT had contaminated the soils water and livestock ofprevious IRS communities [42]
5 Conclusions
The presence of DDT and its metabolites in environmentalsamples from soils and water of selected study areas hasbeen demonstrated Given that the breakdown productsDDE and DDD are more stable in the environment andhuman matrices and have been implicated in dire effectsurgent action is required This calls for more investmentin surveillance and environmental monitoring in order todevelop effective remediation solutions that will rapidlybreak down this DDT and thereby remove it from the foodchain Furthermore the cradle-to-grave principle of wastemanagement must be applied to this dilemma as the cost ofDDT reintroduction is currently being borne by the publicand given the persistent nature of DDT even unborn childrenwill suffer the consequences of this lapse in environmentalstewardship Hard choices driven by appropriate leadershipmay have to be made which favour a win-win situation forcurrent and future generations
Conflict of Interests
The authors declare that they had no conflict of interests inthe execution of this research
Acknowledgments
The authors acknowledge the support provided by theResearch Support Centre at the University of Zambia Schoolof Medicine (UNZA-SoM) through the Southern AfricanConsortium for Research Excellence (SACORE) Awardno WT087537MA which is part of the African Institu-tions Initiative Grant of the Wellcome Trust (Company no2711000) a charity (no 210183) registered in England andthe National Institutes of Health (NIH) through the Med-ical Education Partnership Initiative (MEPI) ProgrammaticAward no 1R24TW008873 entitled ldquoExpanding Innovative
Multidisciplinary Medical Education in Zambiardquo at UNZA-SoM The authors also thank the University of BotswanaFaculty of Science for making the GC-MS used in the studyavailable
References
[1] E Chizema-Kawesha J M Miller RW Steketee et al ldquoScalingupmalaria control in Zambia progress and impact 2005ndash2008rdquoThe American Journal of Tropical Medicine and Hygiene vol 83no 3 pp 480ndash488 2010
[2] E Chanda F Masaninga M Coleman et al ldquoIntegrated vectormanagement the Zambian experiencerdquoMalaria Journal vol 7no 1 article 164 2008
[3] B Sharp P Van Wyk J B Sikasote P Banda and I Klein-schmidt ldquoMalaria control by residual insecticide spraying inChingola and Chililabombwe Copperbelt Province ZambiardquoTropical Medicine amp International Health vol 7 no 9 pp 732ndash736 2002
[4] W J Rogan and A Chen ldquoHealth risks and benefits of bis(4-chlorophenyl)-111-trichloroethane (DDT)rdquo The Lancet vol366 no 9487 pp 763ndash773 2005
[5] M L H Mabaso B Sharp and C Lengeler ldquoHistorical reviewof malarial control in southern African with emphasis on theuse of indoor residual house-sprayingrdquo Tropical Medicine ampInternational Health vol 9 no 8 pp 846ndash856 2004
[6] V Turusov V Rakitsky and L Tomatis ldquoDichlorodiphenyl-trichloroethane (DDT) ubiquity persistence and risksrdquo Envi-ronmental Health Perspectives vol 110 no 2 pp 125ndash128 2002
[7] A G Smith ldquoHow toxic is DDTrdquoTheLancet vol 356 no 9226pp 267ndash268 2000
[8] ATSDR Toxicological Profile for DDT DDE and DDD ATSDRAtlanta Ga USA 2002
[9] C de Jager N H Aneck-Hahn M S Bornman et al ldquoSpermchromatin integrity in DDT-exposed young men living in amalaria area in the Limpopo Province South Africardquo HumanReproduction vol 24 no 10 pp 2429ndash2438 2009
[10] B Eskenazi J Chevrier L G Rosas et al ldquoThe pine river state-ment human health consequences of DDT userdquo EnvironmentalHealth Perspectives vol 117 no 9 pp 1359ndash1367 2009
[11] S K Sagiv J K Nugent T B Brazelton et al ldquoPrenatalorganochlorine exposure and measures of behavior in infancyusing the Neonatal Behavioral Assessment Scale (NBAS)rdquoEnvironmental Health Perspectives vol 116 no 5 pp 666ndash6732008
[12] F Salazar-Garcıa E Gallardo-Dıaz P Ceron-Mireles DLoomis and V H Borja-Aburto ldquoReproductive effects of occu-pational DDT exposure among male malaria control workersrdquoEnvironmental Health Perspectives vol 112 no 5 pp 542ndash5472004
[13] L Torres-Sanchez S J Rothenberg L Schnaas et al ldquoIn uteropp1015840-DDE exposure and infant neurodevelopment a perinatalcohort in Mexicordquo Environmental Health Perspectives vol 115no 3 pp 435ndash439 2007
[14] L Torres-Sanchez L Schnaas M E Cebrian et al ldquoPrenataldichlorodiphenyldichloroethylene (DDE) exposure and neu-rodevelopment a follow-up from 12 to 30 months of agerdquoNeuroToxicology vol 30 no 6 pp 1162ndash1165 2009
[15] N H Aneck-Hahn G W Schulenburg M S Bornman PFarias andCDe Jager ldquoImpaired semen quality associatedwithenvironmental DDT exposure in young men living in a malaria
Journal of Environmental and Public Health 7
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
Several studies have shown that DDT causes thinningof bird egg shells and finds its way into the food chain ifimproperly handled [6ndash8] It is an endocrine disruptor andhas been shown to cause other human health effects rangingfrom reproductive failure to increased incidences of differentcancers [4 9ndash25] Its main action is through the disruptionof the neurological functions of the brain by disturbingneurotransmitters mimicking Th4 a thyroid hormone anddisturbing the internal signalling system of synapses [21 25ndash35]
Locally 239758 kg of DDT has been used in Zambiasince 2000 with no documented studies being conducted onenvironmental and human exposures [36] Previous studieson DDT exposure in other settings involved historicallyexposed communities and looked mainly at its metabolitesDDE andDDDThe few studies done in South Africa focusedon reproductive outcomes in occupationally exposed malesand some in women [9 15] Given the potential harm thatDDT has been shown to cause in various locations aroundthe world coupled with the HIV pandemic and povertysituation in Zambia it is highly likely that these effects willbe more pronounced in the Zambian population So farno study has been carried out to ascertain the fate of therecently applied DDT in both the environment and humanhealth
To this effect we aimed to carry out an exposureassessment in selected areas of Zambia in order to quantifythe prevalence of DDT and its metabolites in soil andwater around communities where it was recently used Thiswork is part of a broader research project which aims tolink recent DDT exposure to neurodevelopmental outcomesin children of the targeted populations and also evaluateother factors that may be associated with the observedoutcomes
2 Materials and Methods
21 Study Areas The study areas comprised ChawamaChongwe and Mongu selected based on history of pastexposure to DDT in the last three years Chawama wasrandomly selected for this study as it was one of the pilot areaswhere DDT was applied in 2004 and has a very high malariaburden compared to the rest of Lusaka It is a periurban areain the center of Lusaka situated at 1535∘ south latitude 287∘east longitude and 1069meters above the sea level Chongweon the other hand is a rural town east of Lusaka situated at1535∘ south latitude 287∘ east longitude and 1069 metersabove the sea level It was also randomly selected amongamong two other areas Kafue and Mumbwa which are ruraldistricts within a 200 km radius to Lusaka as it was one ofthe areas where DDT was applied commencing in 2008 Incontrast Mongu is a town with a mixed urban and ruralpopulation located west of Lusaka situated at 1525∘ southlatitude 2313∘ east longitude and 1018 meters above the sealevel It was conveniently selected as the control area becausethere is no report of DDT application as part of governmentIRS activities [37] Mongu was selected as the reference areawhile Chawama and Chongwe are the areas where DDT wasapplied
Figure 1 Soil sampling pattern
22 Sampling The sampling for soil andwater in all the studyareas was done during July 2012 Compound samples werecollected from locations in the immediate periphery of thehouses
The inclusion criterion for the areas with recent applica-tion was that the residences should have been sprayed at leastthree times with DDT in the last 10 years
221 Soil A total of 14 soil samples were collected inChongwe (3) Chawama (7) and Mongu (4) In order to dis-cern recent exposure characteristics samples were obtainedfrom the top soil at a depth of 2ndash5 cm using bucket andtube augers depending on the type of soil present in thearea At each sampling point 500 g of the soil sample wascollected and placed in a nontransparent paper bag whichwas put into a plastic bag to avoid leakage In order to ensurerepresentativeness of the soil samples in the study areas azigzag sampling pattern was employed covering the entiresampling area in each community as illustrated in Figure 1
222 Water A total of 14 water samples were collected inChongwe (3) Chawama (7) and Mongu (4) respectivelyThe samples were obtained from various drinking watersources such as shallow wells open streams and communaltaps These samples were obtained using 1-litre water samplebottles which had been triple-rinsed with wash grade ace-tonehexane mixture The bottles had tightly fitted caps andlids to avoid spillages and enough space was allowed at theneck of the bottle to facilitate air exchange
The samples were transported to the Mass SpectrometryUnit in the Department of Chemistry at the University ofBotswana under the United Nations Transport of DangerousGoods (UNTDG) Regulations of 2011 [38] where they werekept in a cold room at sim4∘C until they were extracted andanalysed
23 Sample Extraction and Chemical Analysis231 Soil Samples A slightly modified AOAC Method200701 adapted by Nagel [39 40] using QuEChERS kitswas used for extraction of DDT from soil samples Twenty(20) grams of soil was weighed into a centrifuge tube and12mL of water was added and shaken for 4 hours afterwhich 20mL of acetonitrile was added for homogenization
Journal of Environmental and Public Health 3
The supernatant was thereafter quantitatively transferredto a second centrifuge tube containing 6 g MgSO
4 15 g
NaCl 15 g Na3Citrate dihydrate and 750mg Na
2HCitrate
sesquihydrate Centrifugation was done for 2 minutes at4500 rpm Sample cleanup was achieved by using dispersivesolid phase extraction using cartridges that contained 150mgprimary secondary amine (PSA) 400mg C18EC and 900mgmagnesium sulfate of between 985 and 1015 purity In eachextraction 6mL of supernatant was transferred into an SPEcartridge and shaken for 1 minute before centrifugation for2 minutes at 4500 rpm The organic layer was filtered usinga syringe and a membrane filter (045mm) and then evapo-rated under nitrogen to 1mLThe concentratewas transferredinto a 2mLGC vial and was ready for gas chromatography-mass spectrometry (GC-MS) analysis
232 Water Samples The standard solid phase extraction(SPE) method of conditioning loading washing and elutionwas used for the extraction of DDT from the water samplesThis was achieved using Florisil SPE Cartridges and anAgilent vacuum manifold (VacElut SPS 24) The procedurewas a slight modification of a method developed in thelaboratory for the determination of PCBs in transformer oil[41] Eight (8)millilitres of hexanewas added to condition thecartridge followed by 8mL of deionised water at 1mLminThis was followed by loading 20mL of the water sample at aflow rate of 05mLminThe cartridge was allowed to dry foranother 20 minutes to allow for interaction of the DDT withthe stationary phase
Five (5) millilitres of hexane was eluted through thecartridge to wash off any nonpolar analytes that couldhave bound strongly to the stationary phase Elution ofthe DDT was accomplished by running 10mL of a 5 5 n-hexane acetone mixture The resulting eluate was blowngently under a stream of nitrogen to concentrate it to 05mLand transferred to GC vial for GC-MS analysis
24 GC-MS Conditions An Agilent (Palo Alto CA USA)5975 C series gas chromatograph-quadrupole mass spec-trometer (GC-qMS) system equipped with a selective massdetector was used for analysis The system has capability toperform ion manipulation in the full scan and selected ionmonitoring (SIM) modes It also has two ionization modesthat is electron ionization (EI) and chemical ionization (CI)In this study the SIMmode was used after CI using methaneas a reagent gas Helium was used throughout as a carriergas at a flow rate of 1mLmin The oven program for the GCwas as follows The column was held at 80∘C for 2min andthen ramped at 10∘Cmin up to 270∘C for a total run timeof approximately 30 minutes The injector was held at 270∘CThemass spectrometer was operated in the negative chemicalionization (NCI) mode for soil analysis while the electronionization (EI) mode was used for water sample extractsAll the instrumental settings used were optimized prior toapplication on real sample extracts The Automated MassSpectral Deconvolution and Identification System (AMDIS)by the National Institute for Standards and Technology(NIST) in conjunctionwithMicrosoft Excel was used for data
analysis Extraction efficiencies were determined by analysisof spiked sample extracts with the analytes of interest
25 Quality Control For quality control and assurance pro-cedural blanks were extracted with n-hexane and subjectedto the same extraction procedure as the other samples Thesewere run with every ten samples in addition to field andlaboratory blanks Descriptive statistics were used to describedata and the term tDDT was used to refer to the sum of allDDT and its metabolites DDE and DDD In the presentationof the results however a distinction was made as to whichDDT metabolite was being referred to
26 Ethics Written permits were acquired from theMinistryof Mines andMineral Resources to export the soils and waterinto Botswana for analysis The Botswana Unified RevenueService also gave entry permission for the samples
3 Results
31 DDT Distribution and Validation A summary of vali-dation results derived from 6 point calibration curves withcorresponding regression equations is presented in Table 1
From Table 1 reasonably good extraction efficiencieswere attained using both QuEChERS and SPE extractionsLow detection limits were also estimated in both soil andwater samples and when these are compared to the 1120583gLwhich is the World Health Organization (WHO) MaximumRecommended Limit (MRL) for DDT and its derivatives indrinkingwater theywere found to be low enough for analysis
Results of concentrations of DDT and its metabolites inthe study areas are summarized in Figure 2
Figure 2 shows that all analyteswere present in all the soilsof Chawama and Chongwe However they were all foundto be below the LoDs in Mongu which was our referencearea The concentrations varied in all the study areas butthe highest amounts of DDT at 258 ngg were determinedaround a rural homestead of Chongwe followed by 257 nggin soils collected very close to the exterior walls of a house inChawama Township DDT accounted for 12 of the tDDT inthe soils sampled In some areas the percentage was as highas 27
Inwater the sample analysis results are shown in Figure 3DDT in water was found in 6 out of the 14 sampling
points No DDT above the limits of detection was detectedin water samples fromMongu which was the reference sam-pling site In general the lowest amount of DDT accountedfor 4of the tDDTwhile the highest concentration at 511 nggwas detected around a pit latrine in Chawama Townshiptranslating into 75 of tDDT
4 Discussion
DDT levels were found in significant levels in both water andsoils in the study areas of Zambia These high levels weremost prominent in sites with a history of DDT exposurethrough the IRS program for malaria control No DDTabove the limits of detection was found in the reference
Figure 2 DDTDDE andDDDconcentrations in soil samples fromChawama and Chongwe
0200400600800
10001200
DDT DDE DDD tDDTMetabolite
DDT concentrations in water by location
Chawama blue water ChawamaChawama-Kuku Chawama-Ngwenya DamChongwe-Mulilanduba Chongwe-Choombwa
Con
c (120583
gL)
Figure 3 DDT DDE and DDD concentrations in water samplesfrom Chawama and Chongwe
area In soil from the two Zambian study areas the medianconcentrations were twice or higher than those reported inSpain Uganda and South Africa among selected countrieswhere they were 46 59 and 43 ngg respectively [42ndash44]
It is possible that there might be inherent samplingerrors and that coincidentally both sampled sites with recentexposure could have higher DDT concentrations as foundin this study However given that every effort was made torandomly select the locations and sampling sites it is unlikelythat these sampling errors could be important enough toexplain these resultsWe therefore reasonably argue that whatwas found in this exposure assessment could be from recentexposure
DDT has not been sprayed in Zambia since 2010 whenevidence of mosquito resistance to it began to emerge [45]DDT and its metabolites can persist in soil for 2ndash15 years [8]and therefore the period of recent exposure still falls withinthe half-life brackets for DDT The soil sampling protocolrestricted the depth at which the soil samples were collectedto the A and E horizons which are generally about 06ndash45m
below the surface and typically lose minerals and chemicalsdue to leaching over time [46] The study conducted inKenya by Lalah et al showed that DDT and other pesticidesmetabolize faster at varying rates depending on the soil typedue to environmental factors such as prevailing climaticconditions pH of the soil and the action of microorganismsIt has been shown to degrade even faster in temperateclimates such as the one found in Zambia
DDT has a much longer half-life of up to 150 years inwater and due to its lipophilic nature it tends to gravitatetowards organic material and other such fatty tissues Its veryhigh concentrations in the water bodies where the sampleswere collected were a surprising and alarming result Themedian concentrations of DDT were found to be more thantwo hundred times higher than those recorded inNigeria andSouth Africa at less than 0368 and 2120583gL respectively Thisis against the background in which the WHO has recom-mended a maximum of 1120583gL per 001mgkg of body weightcalculated at the assumption that a 10 kg child drinks up to 1litre per day [47]These results corroborate the findings fromthe 2010 Environmental Council of Zambia (ECZ) audit ofIRS activities which showed lapses in the implementation ofenvironmental safeguards during the spraying exercises [36]
No DDT and its metabolites above detectable limits weredetected in the reference area in both soil and water samplesMongu was not included in the IRS program due to itsproximity to the Zambezi River a source of livelihood andnutrition for the local communities Despite the historicalapplication of DDT in the 1940s to the 1980s for otherpurposes in Mongu the sampling of only elluvium A top soilcould havemasked residues whichmost likelymay be presentin the lower strata Given the rapid velocity of the water in theZambezi River and the high water table inMongu it is highlyunlikely thatDDT could have remained in the aquatic systemThis coupled with the presence of many aquatic species andother organic materials in the water bodies in this area couldhave resulted in the DDT sequestering itself in them due toits lipophilicity
These results are clinically significant given the bioaccu-mulation and biomagnification characteristics of DDT as ittravels up the food chain [7 8 47 48] Several studies invarious settings of the world have shown that DDT in plantsis taken up through the roots and when these plants areconsumed by both humans and animals the DDT remainssequestered in these speciesrsquo adipose tissue This is also truewhen DDT sequesters itself in aquatic species which areedible to humans and animals These studies also show thatthe primary exposure route for humans to DDT is throughingestion of contaminated foods and water [47]
The high tDDT concentrations found in the studysites and subsequent DDT contamination burden may bean indication of challenges associated with environmentalmonitoring of such pollutants especially in resource poorsettings already plagued with high malaria incidences amongother public health challenges (Table 2) Given that thesehighly exposed areas are also often inhabited by very poorpopulations most of whom are women and children thisposes an ethical dilemma to decision makers on the cost-effectiveness of reintroducing DDT Speculations were raised
6 Journal of Environmental and Public Health
Table 2 Summary description of tDDT concentrations inChawama and Chongwe
by several scholars on the effectiveness of the reintroductionof DDT formalaria controlThe researchers in [10 49 50] arethus justified This is based on results of studies such as thisone and that conducted in South Africa also which showedthat DDT had contaminated the soils water and livestock ofprevious IRS communities [42]
5 Conclusions
The presence of DDT and its metabolites in environmentalsamples from soils and water of selected study areas hasbeen demonstrated Given that the breakdown productsDDE and DDD are more stable in the environment andhuman matrices and have been implicated in dire effectsurgent action is required This calls for more investmentin surveillance and environmental monitoring in order todevelop effective remediation solutions that will rapidlybreak down this DDT and thereby remove it from the foodchain Furthermore the cradle-to-grave principle of wastemanagement must be applied to this dilemma as the cost ofDDT reintroduction is currently being borne by the publicand given the persistent nature of DDT even unborn childrenwill suffer the consequences of this lapse in environmentalstewardship Hard choices driven by appropriate leadershipmay have to be made which favour a win-win situation forcurrent and future generations
Conflict of Interests
The authors declare that they had no conflict of interests inthe execution of this research
Acknowledgments
The authors acknowledge the support provided by theResearch Support Centre at the University of Zambia Schoolof Medicine (UNZA-SoM) through the Southern AfricanConsortium for Research Excellence (SACORE) Awardno WT087537MA which is part of the African Institu-tions Initiative Grant of the Wellcome Trust (Company no2711000) a charity (no 210183) registered in England andthe National Institutes of Health (NIH) through the Med-ical Education Partnership Initiative (MEPI) ProgrammaticAward no 1R24TW008873 entitled ldquoExpanding Innovative
Multidisciplinary Medical Education in Zambiardquo at UNZA-SoM The authors also thank the University of BotswanaFaculty of Science for making the GC-MS used in the studyavailable
References
[1] E Chizema-Kawesha J M Miller RW Steketee et al ldquoScalingupmalaria control in Zambia progress and impact 2005ndash2008rdquoThe American Journal of Tropical Medicine and Hygiene vol 83no 3 pp 480ndash488 2010
[2] E Chanda F Masaninga M Coleman et al ldquoIntegrated vectormanagement the Zambian experiencerdquoMalaria Journal vol 7no 1 article 164 2008
[3] B Sharp P Van Wyk J B Sikasote P Banda and I Klein-schmidt ldquoMalaria control by residual insecticide spraying inChingola and Chililabombwe Copperbelt Province ZambiardquoTropical Medicine amp International Health vol 7 no 9 pp 732ndash736 2002
[4] W J Rogan and A Chen ldquoHealth risks and benefits of bis(4-chlorophenyl)-111-trichloroethane (DDT)rdquo The Lancet vol366 no 9487 pp 763ndash773 2005
[5] M L H Mabaso B Sharp and C Lengeler ldquoHistorical reviewof malarial control in southern African with emphasis on theuse of indoor residual house-sprayingrdquo Tropical Medicine ampInternational Health vol 9 no 8 pp 846ndash856 2004
[6] V Turusov V Rakitsky and L Tomatis ldquoDichlorodiphenyl-trichloroethane (DDT) ubiquity persistence and risksrdquo Envi-ronmental Health Perspectives vol 110 no 2 pp 125ndash128 2002
[7] A G Smith ldquoHow toxic is DDTrdquoTheLancet vol 356 no 9226pp 267ndash268 2000
[8] ATSDR Toxicological Profile for DDT DDE and DDD ATSDRAtlanta Ga USA 2002
[9] C de Jager N H Aneck-Hahn M S Bornman et al ldquoSpermchromatin integrity in DDT-exposed young men living in amalaria area in the Limpopo Province South Africardquo HumanReproduction vol 24 no 10 pp 2429ndash2438 2009
[10] B Eskenazi J Chevrier L G Rosas et al ldquoThe pine river state-ment human health consequences of DDT userdquo EnvironmentalHealth Perspectives vol 117 no 9 pp 1359ndash1367 2009
[11] S K Sagiv J K Nugent T B Brazelton et al ldquoPrenatalorganochlorine exposure and measures of behavior in infancyusing the Neonatal Behavioral Assessment Scale (NBAS)rdquoEnvironmental Health Perspectives vol 116 no 5 pp 666ndash6732008
[12] F Salazar-Garcıa E Gallardo-Dıaz P Ceron-Mireles DLoomis and V H Borja-Aburto ldquoReproductive effects of occu-pational DDT exposure among male malaria control workersrdquoEnvironmental Health Perspectives vol 112 no 5 pp 542ndash5472004
[13] L Torres-Sanchez S J Rothenberg L Schnaas et al ldquoIn uteropp1015840-DDE exposure and infant neurodevelopment a perinatalcohort in Mexicordquo Environmental Health Perspectives vol 115no 3 pp 435ndash439 2007
[14] L Torres-Sanchez L Schnaas M E Cebrian et al ldquoPrenataldichlorodiphenyldichloroethylene (DDE) exposure and neu-rodevelopment a follow-up from 12 to 30 months of agerdquoNeuroToxicology vol 30 no 6 pp 1162ndash1165 2009
[15] N H Aneck-Hahn G W Schulenburg M S Bornman PFarias andCDe Jager ldquoImpaired semen quality associatedwithenvironmental DDT exposure in young men living in a malaria
Journal of Environmental and Public Health 7
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
The supernatant was thereafter quantitatively transferredto a second centrifuge tube containing 6 g MgSO
4 15 g
NaCl 15 g Na3Citrate dihydrate and 750mg Na
2HCitrate
sesquihydrate Centrifugation was done for 2 minutes at4500 rpm Sample cleanup was achieved by using dispersivesolid phase extraction using cartridges that contained 150mgprimary secondary amine (PSA) 400mg C18EC and 900mgmagnesium sulfate of between 985 and 1015 purity In eachextraction 6mL of supernatant was transferred into an SPEcartridge and shaken for 1 minute before centrifugation for2 minutes at 4500 rpm The organic layer was filtered usinga syringe and a membrane filter (045mm) and then evapo-rated under nitrogen to 1mLThe concentratewas transferredinto a 2mLGC vial and was ready for gas chromatography-mass spectrometry (GC-MS) analysis
232 Water Samples The standard solid phase extraction(SPE) method of conditioning loading washing and elutionwas used for the extraction of DDT from the water samplesThis was achieved using Florisil SPE Cartridges and anAgilent vacuum manifold (VacElut SPS 24) The procedurewas a slight modification of a method developed in thelaboratory for the determination of PCBs in transformer oil[41] Eight (8)millilitres of hexanewas added to condition thecartridge followed by 8mL of deionised water at 1mLminThis was followed by loading 20mL of the water sample at aflow rate of 05mLminThe cartridge was allowed to dry foranother 20 minutes to allow for interaction of the DDT withthe stationary phase
Five (5) millilitres of hexane was eluted through thecartridge to wash off any nonpolar analytes that couldhave bound strongly to the stationary phase Elution ofthe DDT was accomplished by running 10mL of a 5 5 n-hexane acetone mixture The resulting eluate was blowngently under a stream of nitrogen to concentrate it to 05mLand transferred to GC vial for GC-MS analysis
24 GC-MS Conditions An Agilent (Palo Alto CA USA)5975 C series gas chromatograph-quadrupole mass spec-trometer (GC-qMS) system equipped with a selective massdetector was used for analysis The system has capability toperform ion manipulation in the full scan and selected ionmonitoring (SIM) modes It also has two ionization modesthat is electron ionization (EI) and chemical ionization (CI)In this study the SIMmode was used after CI using methaneas a reagent gas Helium was used throughout as a carriergas at a flow rate of 1mLmin The oven program for the GCwas as follows The column was held at 80∘C for 2min andthen ramped at 10∘Cmin up to 270∘C for a total run timeof approximately 30 minutes The injector was held at 270∘CThemass spectrometer was operated in the negative chemicalionization (NCI) mode for soil analysis while the electronionization (EI) mode was used for water sample extractsAll the instrumental settings used were optimized prior toapplication on real sample extracts The Automated MassSpectral Deconvolution and Identification System (AMDIS)by the National Institute for Standards and Technology(NIST) in conjunctionwithMicrosoft Excel was used for data
analysis Extraction efficiencies were determined by analysisof spiked sample extracts with the analytes of interest
25 Quality Control For quality control and assurance pro-cedural blanks were extracted with n-hexane and subjectedto the same extraction procedure as the other samples Thesewere run with every ten samples in addition to field andlaboratory blanks Descriptive statistics were used to describedata and the term tDDT was used to refer to the sum of allDDT and its metabolites DDE and DDD In the presentationof the results however a distinction was made as to whichDDT metabolite was being referred to
26 Ethics Written permits were acquired from theMinistryof Mines andMineral Resources to export the soils and waterinto Botswana for analysis The Botswana Unified RevenueService also gave entry permission for the samples
3 Results
31 DDT Distribution and Validation A summary of vali-dation results derived from 6 point calibration curves withcorresponding regression equations is presented in Table 1
From Table 1 reasonably good extraction efficiencieswere attained using both QuEChERS and SPE extractionsLow detection limits were also estimated in both soil andwater samples and when these are compared to the 1120583gLwhich is the World Health Organization (WHO) MaximumRecommended Limit (MRL) for DDT and its derivatives indrinkingwater theywere found to be low enough for analysis
Results of concentrations of DDT and its metabolites inthe study areas are summarized in Figure 2
Figure 2 shows that all analyteswere present in all the soilsof Chawama and Chongwe However they were all foundto be below the LoDs in Mongu which was our referencearea The concentrations varied in all the study areas butthe highest amounts of DDT at 258 ngg were determinedaround a rural homestead of Chongwe followed by 257 nggin soils collected very close to the exterior walls of a house inChawama Township DDT accounted for 12 of the tDDT inthe soils sampled In some areas the percentage was as highas 27
Inwater the sample analysis results are shown in Figure 3DDT in water was found in 6 out of the 14 sampling
points No DDT above the limits of detection was detectedin water samples fromMongu which was the reference sam-pling site In general the lowest amount of DDT accountedfor 4of the tDDTwhile the highest concentration at 511 nggwas detected around a pit latrine in Chawama Townshiptranslating into 75 of tDDT
4 Discussion
DDT levels were found in significant levels in both water andsoils in the study areas of Zambia These high levels weremost prominent in sites with a history of DDT exposurethrough the IRS program for malaria control No DDTabove the limits of detection was found in the reference
Figure 2 DDTDDE andDDDconcentrations in soil samples fromChawama and Chongwe
0200400600800
10001200
DDT DDE DDD tDDTMetabolite
DDT concentrations in water by location
Chawama blue water ChawamaChawama-Kuku Chawama-Ngwenya DamChongwe-Mulilanduba Chongwe-Choombwa
Con
c (120583
gL)
Figure 3 DDT DDE and DDD concentrations in water samplesfrom Chawama and Chongwe
area In soil from the two Zambian study areas the medianconcentrations were twice or higher than those reported inSpain Uganda and South Africa among selected countrieswhere they were 46 59 and 43 ngg respectively [42ndash44]
It is possible that there might be inherent samplingerrors and that coincidentally both sampled sites with recentexposure could have higher DDT concentrations as foundin this study However given that every effort was made torandomly select the locations and sampling sites it is unlikelythat these sampling errors could be important enough toexplain these resultsWe therefore reasonably argue that whatwas found in this exposure assessment could be from recentexposure
DDT has not been sprayed in Zambia since 2010 whenevidence of mosquito resistance to it began to emerge [45]DDT and its metabolites can persist in soil for 2ndash15 years [8]and therefore the period of recent exposure still falls withinthe half-life brackets for DDT The soil sampling protocolrestricted the depth at which the soil samples were collectedto the A and E horizons which are generally about 06ndash45m
below the surface and typically lose minerals and chemicalsdue to leaching over time [46] The study conducted inKenya by Lalah et al showed that DDT and other pesticidesmetabolize faster at varying rates depending on the soil typedue to environmental factors such as prevailing climaticconditions pH of the soil and the action of microorganismsIt has been shown to degrade even faster in temperateclimates such as the one found in Zambia
DDT has a much longer half-life of up to 150 years inwater and due to its lipophilic nature it tends to gravitatetowards organic material and other such fatty tissues Its veryhigh concentrations in the water bodies where the sampleswere collected were a surprising and alarming result Themedian concentrations of DDT were found to be more thantwo hundred times higher than those recorded inNigeria andSouth Africa at less than 0368 and 2120583gL respectively Thisis against the background in which the WHO has recom-mended a maximum of 1120583gL per 001mgkg of body weightcalculated at the assumption that a 10 kg child drinks up to 1litre per day [47]These results corroborate the findings fromthe 2010 Environmental Council of Zambia (ECZ) audit ofIRS activities which showed lapses in the implementation ofenvironmental safeguards during the spraying exercises [36]
No DDT and its metabolites above detectable limits weredetected in the reference area in both soil and water samplesMongu was not included in the IRS program due to itsproximity to the Zambezi River a source of livelihood andnutrition for the local communities Despite the historicalapplication of DDT in the 1940s to the 1980s for otherpurposes in Mongu the sampling of only elluvium A top soilcould havemasked residues whichmost likelymay be presentin the lower strata Given the rapid velocity of the water in theZambezi River and the high water table inMongu it is highlyunlikely thatDDT could have remained in the aquatic systemThis coupled with the presence of many aquatic species andother organic materials in the water bodies in this area couldhave resulted in the DDT sequestering itself in them due toits lipophilicity
These results are clinically significant given the bioaccu-mulation and biomagnification characteristics of DDT as ittravels up the food chain [7 8 47 48] Several studies invarious settings of the world have shown that DDT in plantsis taken up through the roots and when these plants areconsumed by both humans and animals the DDT remainssequestered in these speciesrsquo adipose tissue This is also truewhen DDT sequesters itself in aquatic species which areedible to humans and animals These studies also show thatthe primary exposure route for humans to DDT is throughingestion of contaminated foods and water [47]
The high tDDT concentrations found in the studysites and subsequent DDT contamination burden may bean indication of challenges associated with environmentalmonitoring of such pollutants especially in resource poorsettings already plagued with high malaria incidences amongother public health challenges (Table 2) Given that thesehighly exposed areas are also often inhabited by very poorpopulations most of whom are women and children thisposes an ethical dilemma to decision makers on the cost-effectiveness of reintroducing DDT Speculations were raised
6 Journal of Environmental and Public Health
Table 2 Summary description of tDDT concentrations inChawama and Chongwe
by several scholars on the effectiveness of the reintroductionof DDT formalaria controlThe researchers in [10 49 50] arethus justified This is based on results of studies such as thisone and that conducted in South Africa also which showedthat DDT had contaminated the soils water and livestock ofprevious IRS communities [42]
5 Conclusions
The presence of DDT and its metabolites in environmentalsamples from soils and water of selected study areas hasbeen demonstrated Given that the breakdown productsDDE and DDD are more stable in the environment andhuman matrices and have been implicated in dire effectsurgent action is required This calls for more investmentin surveillance and environmental monitoring in order todevelop effective remediation solutions that will rapidlybreak down this DDT and thereby remove it from the foodchain Furthermore the cradle-to-grave principle of wastemanagement must be applied to this dilemma as the cost ofDDT reintroduction is currently being borne by the publicand given the persistent nature of DDT even unborn childrenwill suffer the consequences of this lapse in environmentalstewardship Hard choices driven by appropriate leadershipmay have to be made which favour a win-win situation forcurrent and future generations
Conflict of Interests
The authors declare that they had no conflict of interests inthe execution of this research
Acknowledgments
The authors acknowledge the support provided by theResearch Support Centre at the University of Zambia Schoolof Medicine (UNZA-SoM) through the Southern AfricanConsortium for Research Excellence (SACORE) Awardno WT087537MA which is part of the African Institu-tions Initiative Grant of the Wellcome Trust (Company no2711000) a charity (no 210183) registered in England andthe National Institutes of Health (NIH) through the Med-ical Education Partnership Initiative (MEPI) ProgrammaticAward no 1R24TW008873 entitled ldquoExpanding Innovative
Multidisciplinary Medical Education in Zambiardquo at UNZA-SoM The authors also thank the University of BotswanaFaculty of Science for making the GC-MS used in the studyavailable
References
[1] E Chizema-Kawesha J M Miller RW Steketee et al ldquoScalingupmalaria control in Zambia progress and impact 2005ndash2008rdquoThe American Journal of Tropical Medicine and Hygiene vol 83no 3 pp 480ndash488 2010
[2] E Chanda F Masaninga M Coleman et al ldquoIntegrated vectormanagement the Zambian experiencerdquoMalaria Journal vol 7no 1 article 164 2008
[3] B Sharp P Van Wyk J B Sikasote P Banda and I Klein-schmidt ldquoMalaria control by residual insecticide spraying inChingola and Chililabombwe Copperbelt Province ZambiardquoTropical Medicine amp International Health vol 7 no 9 pp 732ndash736 2002
[4] W J Rogan and A Chen ldquoHealth risks and benefits of bis(4-chlorophenyl)-111-trichloroethane (DDT)rdquo The Lancet vol366 no 9487 pp 763ndash773 2005
[5] M L H Mabaso B Sharp and C Lengeler ldquoHistorical reviewof malarial control in southern African with emphasis on theuse of indoor residual house-sprayingrdquo Tropical Medicine ampInternational Health vol 9 no 8 pp 846ndash856 2004
[6] V Turusov V Rakitsky and L Tomatis ldquoDichlorodiphenyl-trichloroethane (DDT) ubiquity persistence and risksrdquo Envi-ronmental Health Perspectives vol 110 no 2 pp 125ndash128 2002
[7] A G Smith ldquoHow toxic is DDTrdquoTheLancet vol 356 no 9226pp 267ndash268 2000
[8] ATSDR Toxicological Profile for DDT DDE and DDD ATSDRAtlanta Ga USA 2002
[9] C de Jager N H Aneck-Hahn M S Bornman et al ldquoSpermchromatin integrity in DDT-exposed young men living in amalaria area in the Limpopo Province South Africardquo HumanReproduction vol 24 no 10 pp 2429ndash2438 2009
[10] B Eskenazi J Chevrier L G Rosas et al ldquoThe pine river state-ment human health consequences of DDT userdquo EnvironmentalHealth Perspectives vol 117 no 9 pp 1359ndash1367 2009
[11] S K Sagiv J K Nugent T B Brazelton et al ldquoPrenatalorganochlorine exposure and measures of behavior in infancyusing the Neonatal Behavioral Assessment Scale (NBAS)rdquoEnvironmental Health Perspectives vol 116 no 5 pp 666ndash6732008
[12] F Salazar-Garcıa E Gallardo-Dıaz P Ceron-Mireles DLoomis and V H Borja-Aburto ldquoReproductive effects of occu-pational DDT exposure among male malaria control workersrdquoEnvironmental Health Perspectives vol 112 no 5 pp 542ndash5472004
[13] L Torres-Sanchez S J Rothenberg L Schnaas et al ldquoIn uteropp1015840-DDE exposure and infant neurodevelopment a perinatalcohort in Mexicordquo Environmental Health Perspectives vol 115no 3 pp 435ndash439 2007
[14] L Torres-Sanchez L Schnaas M E Cebrian et al ldquoPrenataldichlorodiphenyldichloroethylene (DDE) exposure and neu-rodevelopment a follow-up from 12 to 30 months of agerdquoNeuroToxicology vol 30 no 6 pp 1162ndash1165 2009
[15] N H Aneck-Hahn G W Schulenburg M S Bornman PFarias andCDe Jager ldquoImpaired semen quality associatedwithenvironmental DDT exposure in young men living in a malaria
Journal of Environmental and Public Health 7
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
Figure 2 DDTDDE andDDDconcentrations in soil samples fromChawama and Chongwe
0200400600800
10001200
DDT DDE DDD tDDTMetabolite
DDT concentrations in water by location
Chawama blue water ChawamaChawama-Kuku Chawama-Ngwenya DamChongwe-Mulilanduba Chongwe-Choombwa
Con
c (120583
gL)
Figure 3 DDT DDE and DDD concentrations in water samplesfrom Chawama and Chongwe
area In soil from the two Zambian study areas the medianconcentrations were twice or higher than those reported inSpain Uganda and South Africa among selected countrieswhere they were 46 59 and 43 ngg respectively [42ndash44]
It is possible that there might be inherent samplingerrors and that coincidentally both sampled sites with recentexposure could have higher DDT concentrations as foundin this study However given that every effort was made torandomly select the locations and sampling sites it is unlikelythat these sampling errors could be important enough toexplain these resultsWe therefore reasonably argue that whatwas found in this exposure assessment could be from recentexposure
DDT has not been sprayed in Zambia since 2010 whenevidence of mosquito resistance to it began to emerge [45]DDT and its metabolites can persist in soil for 2ndash15 years [8]and therefore the period of recent exposure still falls withinthe half-life brackets for DDT The soil sampling protocolrestricted the depth at which the soil samples were collectedto the A and E horizons which are generally about 06ndash45m
below the surface and typically lose minerals and chemicalsdue to leaching over time [46] The study conducted inKenya by Lalah et al showed that DDT and other pesticidesmetabolize faster at varying rates depending on the soil typedue to environmental factors such as prevailing climaticconditions pH of the soil and the action of microorganismsIt has been shown to degrade even faster in temperateclimates such as the one found in Zambia
DDT has a much longer half-life of up to 150 years inwater and due to its lipophilic nature it tends to gravitatetowards organic material and other such fatty tissues Its veryhigh concentrations in the water bodies where the sampleswere collected were a surprising and alarming result Themedian concentrations of DDT were found to be more thantwo hundred times higher than those recorded inNigeria andSouth Africa at less than 0368 and 2120583gL respectively Thisis against the background in which the WHO has recom-mended a maximum of 1120583gL per 001mgkg of body weightcalculated at the assumption that a 10 kg child drinks up to 1litre per day [47]These results corroborate the findings fromthe 2010 Environmental Council of Zambia (ECZ) audit ofIRS activities which showed lapses in the implementation ofenvironmental safeguards during the spraying exercises [36]
No DDT and its metabolites above detectable limits weredetected in the reference area in both soil and water samplesMongu was not included in the IRS program due to itsproximity to the Zambezi River a source of livelihood andnutrition for the local communities Despite the historicalapplication of DDT in the 1940s to the 1980s for otherpurposes in Mongu the sampling of only elluvium A top soilcould havemasked residues whichmost likelymay be presentin the lower strata Given the rapid velocity of the water in theZambezi River and the high water table inMongu it is highlyunlikely thatDDT could have remained in the aquatic systemThis coupled with the presence of many aquatic species andother organic materials in the water bodies in this area couldhave resulted in the DDT sequestering itself in them due toits lipophilicity
These results are clinically significant given the bioaccu-mulation and biomagnification characteristics of DDT as ittravels up the food chain [7 8 47 48] Several studies invarious settings of the world have shown that DDT in plantsis taken up through the roots and when these plants areconsumed by both humans and animals the DDT remainssequestered in these speciesrsquo adipose tissue This is also truewhen DDT sequesters itself in aquatic species which areedible to humans and animals These studies also show thatthe primary exposure route for humans to DDT is throughingestion of contaminated foods and water [47]
The high tDDT concentrations found in the studysites and subsequent DDT contamination burden may bean indication of challenges associated with environmentalmonitoring of such pollutants especially in resource poorsettings already plagued with high malaria incidences amongother public health challenges (Table 2) Given that thesehighly exposed areas are also often inhabited by very poorpopulations most of whom are women and children thisposes an ethical dilemma to decision makers on the cost-effectiveness of reintroducing DDT Speculations were raised
6 Journal of Environmental and Public Health
Table 2 Summary description of tDDT concentrations inChawama and Chongwe
by several scholars on the effectiveness of the reintroductionof DDT formalaria controlThe researchers in [10 49 50] arethus justified This is based on results of studies such as thisone and that conducted in South Africa also which showedthat DDT had contaminated the soils water and livestock ofprevious IRS communities [42]
5 Conclusions
The presence of DDT and its metabolites in environmentalsamples from soils and water of selected study areas hasbeen demonstrated Given that the breakdown productsDDE and DDD are more stable in the environment andhuman matrices and have been implicated in dire effectsurgent action is required This calls for more investmentin surveillance and environmental monitoring in order todevelop effective remediation solutions that will rapidlybreak down this DDT and thereby remove it from the foodchain Furthermore the cradle-to-grave principle of wastemanagement must be applied to this dilemma as the cost ofDDT reintroduction is currently being borne by the publicand given the persistent nature of DDT even unborn childrenwill suffer the consequences of this lapse in environmentalstewardship Hard choices driven by appropriate leadershipmay have to be made which favour a win-win situation forcurrent and future generations
Conflict of Interests
The authors declare that they had no conflict of interests inthe execution of this research
Acknowledgments
The authors acknowledge the support provided by theResearch Support Centre at the University of Zambia Schoolof Medicine (UNZA-SoM) through the Southern AfricanConsortium for Research Excellence (SACORE) Awardno WT087537MA which is part of the African Institu-tions Initiative Grant of the Wellcome Trust (Company no2711000) a charity (no 210183) registered in England andthe National Institutes of Health (NIH) through the Med-ical Education Partnership Initiative (MEPI) ProgrammaticAward no 1R24TW008873 entitled ldquoExpanding Innovative
Multidisciplinary Medical Education in Zambiardquo at UNZA-SoM The authors also thank the University of BotswanaFaculty of Science for making the GC-MS used in the studyavailable
References
[1] E Chizema-Kawesha J M Miller RW Steketee et al ldquoScalingupmalaria control in Zambia progress and impact 2005ndash2008rdquoThe American Journal of Tropical Medicine and Hygiene vol 83no 3 pp 480ndash488 2010
[2] E Chanda F Masaninga M Coleman et al ldquoIntegrated vectormanagement the Zambian experiencerdquoMalaria Journal vol 7no 1 article 164 2008
[3] B Sharp P Van Wyk J B Sikasote P Banda and I Klein-schmidt ldquoMalaria control by residual insecticide spraying inChingola and Chililabombwe Copperbelt Province ZambiardquoTropical Medicine amp International Health vol 7 no 9 pp 732ndash736 2002
[4] W J Rogan and A Chen ldquoHealth risks and benefits of bis(4-chlorophenyl)-111-trichloroethane (DDT)rdquo The Lancet vol366 no 9487 pp 763ndash773 2005
[5] M L H Mabaso B Sharp and C Lengeler ldquoHistorical reviewof malarial control in southern African with emphasis on theuse of indoor residual house-sprayingrdquo Tropical Medicine ampInternational Health vol 9 no 8 pp 846ndash856 2004
[6] V Turusov V Rakitsky and L Tomatis ldquoDichlorodiphenyl-trichloroethane (DDT) ubiquity persistence and risksrdquo Envi-ronmental Health Perspectives vol 110 no 2 pp 125ndash128 2002
[7] A G Smith ldquoHow toxic is DDTrdquoTheLancet vol 356 no 9226pp 267ndash268 2000
[8] ATSDR Toxicological Profile for DDT DDE and DDD ATSDRAtlanta Ga USA 2002
[9] C de Jager N H Aneck-Hahn M S Bornman et al ldquoSpermchromatin integrity in DDT-exposed young men living in amalaria area in the Limpopo Province South Africardquo HumanReproduction vol 24 no 10 pp 2429ndash2438 2009
[10] B Eskenazi J Chevrier L G Rosas et al ldquoThe pine river state-ment human health consequences of DDT userdquo EnvironmentalHealth Perspectives vol 117 no 9 pp 1359ndash1367 2009
[11] S K Sagiv J K Nugent T B Brazelton et al ldquoPrenatalorganochlorine exposure and measures of behavior in infancyusing the Neonatal Behavioral Assessment Scale (NBAS)rdquoEnvironmental Health Perspectives vol 116 no 5 pp 666ndash6732008
[12] F Salazar-Garcıa E Gallardo-Dıaz P Ceron-Mireles DLoomis and V H Borja-Aburto ldquoReproductive effects of occu-pational DDT exposure among male malaria control workersrdquoEnvironmental Health Perspectives vol 112 no 5 pp 542ndash5472004
[13] L Torres-Sanchez S J Rothenberg L Schnaas et al ldquoIn uteropp1015840-DDE exposure and infant neurodevelopment a perinatalcohort in Mexicordquo Environmental Health Perspectives vol 115no 3 pp 435ndash439 2007
[14] L Torres-Sanchez L Schnaas M E Cebrian et al ldquoPrenataldichlorodiphenyldichloroethylene (DDE) exposure and neu-rodevelopment a follow-up from 12 to 30 months of agerdquoNeuroToxicology vol 30 no 6 pp 1162ndash1165 2009
[15] N H Aneck-Hahn G W Schulenburg M S Bornman PFarias andCDe Jager ldquoImpaired semen quality associatedwithenvironmental DDT exposure in young men living in a malaria
Journal of Environmental and Public Health 7
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
Figure 2 DDTDDE andDDDconcentrations in soil samples fromChawama and Chongwe
0200400600800
10001200
DDT DDE DDD tDDTMetabolite
DDT concentrations in water by location
Chawama blue water ChawamaChawama-Kuku Chawama-Ngwenya DamChongwe-Mulilanduba Chongwe-Choombwa
Con
c (120583
gL)
Figure 3 DDT DDE and DDD concentrations in water samplesfrom Chawama and Chongwe
area In soil from the two Zambian study areas the medianconcentrations were twice or higher than those reported inSpain Uganda and South Africa among selected countrieswhere they were 46 59 and 43 ngg respectively [42ndash44]
It is possible that there might be inherent samplingerrors and that coincidentally both sampled sites with recentexposure could have higher DDT concentrations as foundin this study However given that every effort was made torandomly select the locations and sampling sites it is unlikelythat these sampling errors could be important enough toexplain these resultsWe therefore reasonably argue that whatwas found in this exposure assessment could be from recentexposure
DDT has not been sprayed in Zambia since 2010 whenevidence of mosquito resistance to it began to emerge [45]DDT and its metabolites can persist in soil for 2ndash15 years [8]and therefore the period of recent exposure still falls withinthe half-life brackets for DDT The soil sampling protocolrestricted the depth at which the soil samples were collectedto the A and E horizons which are generally about 06ndash45m
below the surface and typically lose minerals and chemicalsdue to leaching over time [46] The study conducted inKenya by Lalah et al showed that DDT and other pesticidesmetabolize faster at varying rates depending on the soil typedue to environmental factors such as prevailing climaticconditions pH of the soil and the action of microorganismsIt has been shown to degrade even faster in temperateclimates such as the one found in Zambia
DDT has a much longer half-life of up to 150 years inwater and due to its lipophilic nature it tends to gravitatetowards organic material and other such fatty tissues Its veryhigh concentrations in the water bodies where the sampleswere collected were a surprising and alarming result Themedian concentrations of DDT were found to be more thantwo hundred times higher than those recorded inNigeria andSouth Africa at less than 0368 and 2120583gL respectively Thisis against the background in which the WHO has recom-mended a maximum of 1120583gL per 001mgkg of body weightcalculated at the assumption that a 10 kg child drinks up to 1litre per day [47]These results corroborate the findings fromthe 2010 Environmental Council of Zambia (ECZ) audit ofIRS activities which showed lapses in the implementation ofenvironmental safeguards during the spraying exercises [36]
No DDT and its metabolites above detectable limits weredetected in the reference area in both soil and water samplesMongu was not included in the IRS program due to itsproximity to the Zambezi River a source of livelihood andnutrition for the local communities Despite the historicalapplication of DDT in the 1940s to the 1980s for otherpurposes in Mongu the sampling of only elluvium A top soilcould havemasked residues whichmost likelymay be presentin the lower strata Given the rapid velocity of the water in theZambezi River and the high water table inMongu it is highlyunlikely thatDDT could have remained in the aquatic systemThis coupled with the presence of many aquatic species andother organic materials in the water bodies in this area couldhave resulted in the DDT sequestering itself in them due toits lipophilicity
These results are clinically significant given the bioaccu-mulation and biomagnification characteristics of DDT as ittravels up the food chain [7 8 47 48] Several studies invarious settings of the world have shown that DDT in plantsis taken up through the roots and when these plants areconsumed by both humans and animals the DDT remainssequestered in these speciesrsquo adipose tissue This is also truewhen DDT sequesters itself in aquatic species which areedible to humans and animals These studies also show thatthe primary exposure route for humans to DDT is throughingestion of contaminated foods and water [47]
The high tDDT concentrations found in the studysites and subsequent DDT contamination burden may bean indication of challenges associated with environmentalmonitoring of such pollutants especially in resource poorsettings already plagued with high malaria incidences amongother public health challenges (Table 2) Given that thesehighly exposed areas are also often inhabited by very poorpopulations most of whom are women and children thisposes an ethical dilemma to decision makers on the cost-effectiveness of reintroducing DDT Speculations were raised
6 Journal of Environmental and Public Health
Table 2 Summary description of tDDT concentrations inChawama and Chongwe
by several scholars on the effectiveness of the reintroductionof DDT formalaria controlThe researchers in [10 49 50] arethus justified This is based on results of studies such as thisone and that conducted in South Africa also which showedthat DDT had contaminated the soils water and livestock ofprevious IRS communities [42]
5 Conclusions
The presence of DDT and its metabolites in environmentalsamples from soils and water of selected study areas hasbeen demonstrated Given that the breakdown productsDDE and DDD are more stable in the environment andhuman matrices and have been implicated in dire effectsurgent action is required This calls for more investmentin surveillance and environmental monitoring in order todevelop effective remediation solutions that will rapidlybreak down this DDT and thereby remove it from the foodchain Furthermore the cradle-to-grave principle of wastemanagement must be applied to this dilemma as the cost ofDDT reintroduction is currently being borne by the publicand given the persistent nature of DDT even unborn childrenwill suffer the consequences of this lapse in environmentalstewardship Hard choices driven by appropriate leadershipmay have to be made which favour a win-win situation forcurrent and future generations
Conflict of Interests
The authors declare that they had no conflict of interests inthe execution of this research
Acknowledgments
The authors acknowledge the support provided by theResearch Support Centre at the University of Zambia Schoolof Medicine (UNZA-SoM) through the Southern AfricanConsortium for Research Excellence (SACORE) Awardno WT087537MA which is part of the African Institu-tions Initiative Grant of the Wellcome Trust (Company no2711000) a charity (no 210183) registered in England andthe National Institutes of Health (NIH) through the Med-ical Education Partnership Initiative (MEPI) ProgrammaticAward no 1R24TW008873 entitled ldquoExpanding Innovative
Multidisciplinary Medical Education in Zambiardquo at UNZA-SoM The authors also thank the University of BotswanaFaculty of Science for making the GC-MS used in the studyavailable
References
[1] E Chizema-Kawesha J M Miller RW Steketee et al ldquoScalingupmalaria control in Zambia progress and impact 2005ndash2008rdquoThe American Journal of Tropical Medicine and Hygiene vol 83no 3 pp 480ndash488 2010
[2] E Chanda F Masaninga M Coleman et al ldquoIntegrated vectormanagement the Zambian experiencerdquoMalaria Journal vol 7no 1 article 164 2008
[3] B Sharp P Van Wyk J B Sikasote P Banda and I Klein-schmidt ldquoMalaria control by residual insecticide spraying inChingola and Chililabombwe Copperbelt Province ZambiardquoTropical Medicine amp International Health vol 7 no 9 pp 732ndash736 2002
[4] W J Rogan and A Chen ldquoHealth risks and benefits of bis(4-chlorophenyl)-111-trichloroethane (DDT)rdquo The Lancet vol366 no 9487 pp 763ndash773 2005
[5] M L H Mabaso B Sharp and C Lengeler ldquoHistorical reviewof malarial control in southern African with emphasis on theuse of indoor residual house-sprayingrdquo Tropical Medicine ampInternational Health vol 9 no 8 pp 846ndash856 2004
[6] V Turusov V Rakitsky and L Tomatis ldquoDichlorodiphenyl-trichloroethane (DDT) ubiquity persistence and risksrdquo Envi-ronmental Health Perspectives vol 110 no 2 pp 125ndash128 2002
[7] A G Smith ldquoHow toxic is DDTrdquoTheLancet vol 356 no 9226pp 267ndash268 2000
[8] ATSDR Toxicological Profile for DDT DDE and DDD ATSDRAtlanta Ga USA 2002
[9] C de Jager N H Aneck-Hahn M S Bornman et al ldquoSpermchromatin integrity in DDT-exposed young men living in amalaria area in the Limpopo Province South Africardquo HumanReproduction vol 24 no 10 pp 2429ndash2438 2009
[10] B Eskenazi J Chevrier L G Rosas et al ldquoThe pine river state-ment human health consequences of DDT userdquo EnvironmentalHealth Perspectives vol 117 no 9 pp 1359ndash1367 2009
[11] S K Sagiv J K Nugent T B Brazelton et al ldquoPrenatalorganochlorine exposure and measures of behavior in infancyusing the Neonatal Behavioral Assessment Scale (NBAS)rdquoEnvironmental Health Perspectives vol 116 no 5 pp 666ndash6732008
[12] F Salazar-Garcıa E Gallardo-Dıaz P Ceron-Mireles DLoomis and V H Borja-Aburto ldquoReproductive effects of occu-pational DDT exposure among male malaria control workersrdquoEnvironmental Health Perspectives vol 112 no 5 pp 542ndash5472004
[13] L Torres-Sanchez S J Rothenberg L Schnaas et al ldquoIn uteropp1015840-DDE exposure and infant neurodevelopment a perinatalcohort in Mexicordquo Environmental Health Perspectives vol 115no 3 pp 435ndash439 2007
[14] L Torres-Sanchez L Schnaas M E Cebrian et al ldquoPrenataldichlorodiphenyldichloroethylene (DDE) exposure and neu-rodevelopment a follow-up from 12 to 30 months of agerdquoNeuroToxicology vol 30 no 6 pp 1162ndash1165 2009
[15] N H Aneck-Hahn G W Schulenburg M S Bornman PFarias andCDe Jager ldquoImpaired semen quality associatedwithenvironmental DDT exposure in young men living in a malaria
Journal of Environmental and Public Health 7
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
by several scholars on the effectiveness of the reintroductionof DDT formalaria controlThe researchers in [10 49 50] arethus justified This is based on results of studies such as thisone and that conducted in South Africa also which showedthat DDT had contaminated the soils water and livestock ofprevious IRS communities [42]
5 Conclusions
The presence of DDT and its metabolites in environmentalsamples from soils and water of selected study areas hasbeen demonstrated Given that the breakdown productsDDE and DDD are more stable in the environment andhuman matrices and have been implicated in dire effectsurgent action is required This calls for more investmentin surveillance and environmental monitoring in order todevelop effective remediation solutions that will rapidlybreak down this DDT and thereby remove it from the foodchain Furthermore the cradle-to-grave principle of wastemanagement must be applied to this dilemma as the cost ofDDT reintroduction is currently being borne by the publicand given the persistent nature of DDT even unborn childrenwill suffer the consequences of this lapse in environmentalstewardship Hard choices driven by appropriate leadershipmay have to be made which favour a win-win situation forcurrent and future generations
Conflict of Interests
The authors declare that they had no conflict of interests inthe execution of this research
Acknowledgments
The authors acknowledge the support provided by theResearch Support Centre at the University of Zambia Schoolof Medicine (UNZA-SoM) through the Southern AfricanConsortium for Research Excellence (SACORE) Awardno WT087537MA which is part of the African Institu-tions Initiative Grant of the Wellcome Trust (Company no2711000) a charity (no 210183) registered in England andthe National Institutes of Health (NIH) through the Med-ical Education Partnership Initiative (MEPI) ProgrammaticAward no 1R24TW008873 entitled ldquoExpanding Innovative
Multidisciplinary Medical Education in Zambiardquo at UNZA-SoM The authors also thank the University of BotswanaFaculty of Science for making the GC-MS used in the studyavailable
References
[1] E Chizema-Kawesha J M Miller RW Steketee et al ldquoScalingupmalaria control in Zambia progress and impact 2005ndash2008rdquoThe American Journal of Tropical Medicine and Hygiene vol 83no 3 pp 480ndash488 2010
[2] E Chanda F Masaninga M Coleman et al ldquoIntegrated vectormanagement the Zambian experiencerdquoMalaria Journal vol 7no 1 article 164 2008
[3] B Sharp P Van Wyk J B Sikasote P Banda and I Klein-schmidt ldquoMalaria control by residual insecticide spraying inChingola and Chililabombwe Copperbelt Province ZambiardquoTropical Medicine amp International Health vol 7 no 9 pp 732ndash736 2002
[4] W J Rogan and A Chen ldquoHealth risks and benefits of bis(4-chlorophenyl)-111-trichloroethane (DDT)rdquo The Lancet vol366 no 9487 pp 763ndash773 2005
[5] M L H Mabaso B Sharp and C Lengeler ldquoHistorical reviewof malarial control in southern African with emphasis on theuse of indoor residual house-sprayingrdquo Tropical Medicine ampInternational Health vol 9 no 8 pp 846ndash856 2004
[6] V Turusov V Rakitsky and L Tomatis ldquoDichlorodiphenyl-trichloroethane (DDT) ubiquity persistence and risksrdquo Envi-ronmental Health Perspectives vol 110 no 2 pp 125ndash128 2002
[7] A G Smith ldquoHow toxic is DDTrdquoTheLancet vol 356 no 9226pp 267ndash268 2000
[8] ATSDR Toxicological Profile for DDT DDE and DDD ATSDRAtlanta Ga USA 2002
[9] C de Jager N H Aneck-Hahn M S Bornman et al ldquoSpermchromatin integrity in DDT-exposed young men living in amalaria area in the Limpopo Province South Africardquo HumanReproduction vol 24 no 10 pp 2429ndash2438 2009
[10] B Eskenazi J Chevrier L G Rosas et al ldquoThe pine river state-ment human health consequences of DDT userdquo EnvironmentalHealth Perspectives vol 117 no 9 pp 1359ndash1367 2009
[11] S K Sagiv J K Nugent T B Brazelton et al ldquoPrenatalorganochlorine exposure and measures of behavior in infancyusing the Neonatal Behavioral Assessment Scale (NBAS)rdquoEnvironmental Health Perspectives vol 116 no 5 pp 666ndash6732008
[12] F Salazar-Garcıa E Gallardo-Dıaz P Ceron-Mireles DLoomis and V H Borja-Aburto ldquoReproductive effects of occu-pational DDT exposure among male malaria control workersrdquoEnvironmental Health Perspectives vol 112 no 5 pp 542ndash5472004
[13] L Torres-Sanchez S J Rothenberg L Schnaas et al ldquoIn uteropp1015840-DDE exposure and infant neurodevelopment a perinatalcohort in Mexicordquo Environmental Health Perspectives vol 115no 3 pp 435ndash439 2007
[14] L Torres-Sanchez L Schnaas M E Cebrian et al ldquoPrenataldichlorodiphenyldichloroethylene (DDE) exposure and neu-rodevelopment a follow-up from 12 to 30 months of agerdquoNeuroToxicology vol 30 no 6 pp 1162ndash1165 2009
[15] N H Aneck-Hahn G W Schulenburg M S Bornman PFarias andCDe Jager ldquoImpaired semen quality associatedwithenvironmental DDT exposure in young men living in a malaria
Journal of Environmental and Public Health 7
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
area in the Province South Africardquo Journal of Andrology vol28 no 3 pp 423ndash434 2007
[16] J E Akkina J S Reif T J Keefe and A M Bachand ldquoAge atnatural menopause and exposure to organochlorine pesticidesin hispanic womenrdquo Journal of Toxicology and EnvironmentalHealth Part A vol 67 no 18 pp 1407ndash1422 2004
[17] R Asawasinsopon T Prapamontol O Prakobvitayakit YVaneesorn A Mangklabruks and B Hock ldquoPlasma levels ofDDT and their associationwith reproductive hormones in adultmen from northernThailandrdquo Science of the Total Environmentvol 355 no 1ndash3 pp 98ndash105 2006
[18] P Cocco D Fadda A Ibba et al ldquoReproductive outcomes inDDT applicatorsrdquo Environmental Research vol 98 no 1 pp120ndash126 2005
[19] B A Cohn P M Cirillo M S Wolff et al ldquoDDT and DDEexposure in mothers and time to pregnancy in daughtersrdquo TheLancet vol 361 no 9376 pp 2205ndash2206 2003
[20] B A Cohn M S Wolff P M Cirillo and R I Scholtz ldquoDDTand breast cancer in youngwomen newdata on the significanceof age at exposurerdquo Environmental Health Perspectives vol 115no 10 pp 1406ndash1414 2007
[21] T Colborn ldquoNeurodevelopment and endocrine disruptionrdquoEnvironmental Health Perspectives vol 112 no 9 pp 944ndash9492004
[22] G S Cooper D A Savitz R Millikan and T C Kit ldquoOrgano-chlorine exposure and age at naturalmenopauserdquoEpidemiologyvol 13 no 6 pp 729ndash733 2002
[23] M A Dalvie ldquoDDT health effectsrdquo in Reference Module inEarth Systems and Environmental Sciences Elsevier 2013
[24] D H Garabrant J Held B Langholz J M Peters and T MMack ldquoDDT and related compounds and risk of pancreaticcancerrdquo Journal of the National Cancer Institute vol 84 no 10pp 764ndash771 1992
[25] P R Kodavanti ldquoNeurotoxicity of persistent organic pollutantspossible mode(S) of action and further considerationsrdquo Dose-Response vol 3 no 3 pp 273ndash305 2005
[26] D Rice and S Barone Jr ldquoCritical periods of vulnerability forthe developing nervous system evidence from humans andanimal modelsrdquo Environmental Health Perspectives vol 108supplement 3 pp 511ndash533 2000
[28] I Al-Saleh I Al-Doush A Alsabbaheen G E D Mohamedand A Rabbah ldquoLevels of DDT and its metabolites in pla-centa maternal and cord blood and their potential influenceon neonatal anthropometric measuresrdquo Science of the TotalEnvironment vol 416 pp 62ndash74 2012
[29] B Eskenazi A R Marks A Bradman et al ldquoIn utero exposureto dichlorodiphenyltrichloroethane (DDT) and dichlorodi-phenyldichloroethylene (DDE) and neurodevelopment amongyoung Mexican American childrenrdquo Pediatrics vol 118 no 1pp 233ndash241 2006
[30] B Eskenazi L G Rosas A R Marks et al ldquoPesticide toxicityand the developing brainrdquo Basic amp Clinical Pharmacology ampToxicology vol 102 no 2 pp 228ndash236 2008
[31] B C Gladen and W J Rogan ldquoEffects of perinatal polychlori-nated biphenyls and dichlorodiphenyl dichloroethene on laterdevelopmentrdquoThe Journal of Pediatrics vol 119 no 1 part 1 pp58ndash63 1991
[32] B C Gladen W J Rogan P Hardy J Thullen J Tingelstadand M Tully ldquoDevelopment after exposure to polychlorinated
biphenyls and dichlorodiphenyl dichloroethene transplacen-tally and through human milkrdquo The Journal of Pediatrics vol113 no 6 pp 991ndash995 1988
[33] J Jurewicz and W Hanke ldquoPrenatal and childhood exposureto pesticides and neurobehavioral development review ofepidemiological studiesrdquo International Journal of OccupationalMedicine and Environmental Health vol 21 no 2 pp 121ndash1322008
[34] P Landrigan A Garg and D B J Droller ldquoAssessing theeffects of endocrine disruptors in the national Childrenrsquos studyrdquoEnvironmentalHealth Perspectives vol 111 no 13 pp 1678ndash16822003
[35] L G Rosas and B Eskenazi ldquoPesticides and child neurodevel-opmentrdquo Current Opinion in Pediatrics vol 20 no 2 pp 191ndash197 2008
[36] ECZ Indoor Residual Spraying (IRS) 2010 Environmental Safe-guards Pre Spray Monitoring Report Ministry of TourismEnvironment and Natural Resources Lusaka Zambia 2010
[37] RTI International Environmental Assessment for IRS UsingAlpha-Cypermethrin DDT and Lambda-Cyhalothrin forMalaria Control in Zambia RTI International ResearchTriangle Park NC USA 2006
[38] UNECE Reccommendations on the Transport of DangerousGoods Model Regulations vol 1 UNECE New York NY USA2011
[39] AOAC International AOAC Official Method 200701 PesticideResidues in Foods by Acetonitrile Extraction and Partitioningwith Magnesium Sulfate AOAC International 2007
[40] T Nagel ldquoThe QuEChERS methodmdasha new approach in pes-ticide analysis of soilsrdquo Journal of Horticulture Forestry andBiotechnology vol 13 p 391 2009
[41] S Motladiile H M Kwaambwa and K Sichilongo ldquoDevelop-ment and validation of a gas chromatography-mass spectrom-etry method for the determination of PCBs in transformer oilsamples-application on real samples from Botswanardquo Journal ofChromatography amp Separation Techniques vol 2012 no 4 pp116ndash124 2012
[42] J C Van Dyk H Bouwman I E J Barnhoorn and M SBornman ldquoDDT contamination from indoor residual sprayingfor malaria controlrdquo Science of the Total Environment vol 408no 13 pp 2745ndash2752 2010
[43] P Ssebugere JWasswa J Mbabazi S A Nyanzi B T Kiremireand J A M Marco ldquoOrganochlorine pesticides in soils fromsouth-western Ugandardquo Chemosphere vol 78 no 10 pp 1250ndash1255 2010
[44] R Abrahao J Sarasa J Causape I Garcia-Garizabal and J LOvelleiro ldquoInfluence of irrigation on the occurrence of organicand inorganic pollutants in soil water and sediments of aSpanish agrarian basin (Lerma)rdquo Spanish Journal of AgriculturalResearch vol 9 no 1 pp 124ndash134 2011
[45] E Chanda J Hemingway I Kleinschmidt et al ldquoInsecticideresistance and the future of malaria control in Zambiardquo PLoSONE vol 6 no 9 Article ID e24336 2011
[46] J O Lalah P N Kaigwara Z Getenga J M Mghenyi and SO Wandiga ldquoThe major environmental factors that influencerapid disappearance of pesticides from tropical soils in KenyardquoToxicological amp Environmental Chemistry vol 81 no 3-4 pp161ndash197 2001
[47] WHO ldquoDDT and its derivatives in drinking-water backgrounddocument for development of WHO guidelines for drinking-water qualityrdquo Tech Rep WHOSDEWSH030489 WorldHealth Organization Geneva Switzerland 2004
8 Journal of Environmental and Public Health
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007
[48] J M Ginsburg ldquoPesticide residues in soils accumulation ofDDT in soils from spray practicesrdquo Journal of Agricultural andFood Chemistry vol 3 no 4 pp 322ndash325 1955
[49] H Bouwman H van den Berg and H Kylin ldquoDDT andmalaria prevention addressing the paradoxrdquo EnvironmentalHealth Perspectives vol 119 no 6 pp 744ndash747 2011
[50] R M Guimaraes C I R F Asmus and A Meyer ldquoDDTreintroduction for malaria control the cost-benefit debate forpublic healthrdquo Cadernos de Saude Publica vol 23 no 12 pp2835ndash2844 2007