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Journal of Agromedicine

ISSN: 1059-924X (Print) 1545-0813 (Online) Journal homepage: http://www.tandfonline.com/loi/wagr20

Glyphosate and Paraquat in Maternal and FetalSerums in Thai Women

Pornpimol Kongtip, Noppanun Nankongnab, RatanavadeePhupancharoensuk, Chonlada Palarach, Dusit Sujirarat, Supha Sangprasert,Malasod Sermsuk, Namthip Sawattrakool & Susan Renee Woskie

To cite this article: Pornpimol Kongtip, Noppanun Nankongnab, Ratanavadee Phupancharoensuk,Chonlada Palarach, Dusit Sujirarat, Supha Sangprasert, Malasod Sermsuk, Namthip Sawattrakool& Susan Renee Woskie (2017) Glyphosate and Paraquat in Maternal and Fetal Serums in ThaiWomen, Journal of Agromedicine, 22:3, 282-289, DOI: 10.1080/1059924X.2017.1319315

To link to this article: https://doi.org/10.1080/1059924X.2017.1319315

Accepted author version posted online: 19Apr 2017.Published online: 19 Apr 2017.

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Glyphosate and Paraquat in Maternal and Fetal Serums in Thai WomenPornpimol Kongtipa, Noppanun Nankongnaba, Ratanavadee Phupancharoensuka, Chonlada Palaracha,Dusit Sujiraratb, Supha Sangprasertc, Malasod Sermsukd, Namthip Sawattrakoole, and Susan Renee Woskief

aDepartment of Occupational Health and Safety, Faculty of Public Health, Mahidol University, Center of Excellence on Environmental Healthand Toxicology, Commission on Higher Education, Ministry of Education, Bangkok, Thailand; bDepartment of Epidemiology, Faculty of PublicHealth, Mahidol University, Bangkok, Thailand; cSawanpracharak Hospital, Nakhon Sawan, Thailand; dPaholpolpayuhasena Hospital,Kanchanaburi, Thailand; eAmnatcharoen Hospital, Amnartcharoen, Thailand; fDepartment of Work Environment, University of MassachusettsLowell, Lowell, Massachusetts, USA

ABSTRACTObjectives: This longitudinal study measured the glyphosate and paraquat concentrations foundin maternal and umbilical cord serum in 82 pregnant women who gave birth in three provinces ofThailand. Methods: Through questionnaires and biological samples collected at childbirth, factorssuch as personal characteristics, family members occupation, agricultural activities, and herbicideuse in agricultural work were evaluated as predictors of glyphosate and paraquat levels in thepregnant women. Statistical analysis used univariate and binary multiple logistic regression, wherethe outcome was the probability of exposure to paraquat or glyphosate above the limit ofdetection associated with occupation and household factors. Results: The glyphosate concentra-tions in the pregnant women’s serum at childbirth (median: 17.5, range: 0.2–189.1 ng/mL) weresignificantly higher (P < .007) than those in the umbilical cord serum (median: 0.2, range: 0.2–94.9ng/mL). However, the paraquat concentrations in the serum of the pregnant women at childbirth(83% ≤limit of detection [LOD], with maximum of 58.3 ng/mL) were similar to those in theumbilical cord serum (80% <LOD, with maximum of 47.6 ng/mL). Women with glyphosate levels>LOD in serum at childbirth were 11.9 times more likely to report work as an agriculturist (P <.001), 3.7 times more likely to live near agricultural areas (P = .006), and 5.9 times more likely tohave a family member who worked in agriculture (P < .001). The only factors affecting paraquatexposures in pregnant women at childbirth were reporting the agricultural activity of digging infarm soil and working in the agricultural fields in the third trimester of pregnancy. Conclusions:These results show that pregnant women who work in agriculture or live in families that work inagriculture have higher exposures to the herbicides glyphosate and paraquat. The potential forlong-term health impacts of these prenatal exposures to children should be evaluated, andgreater regulation of the sale and use of herbicides should be considered in Thailand.

KEYWORDSAgricultural activities;glyphosate; maternal andumbilical cord serums;paraquat; pregnant women

Introduction

In Thailand, herbicides are widely used in agricul-ture to increase produce yields and quality. Datafrom the Thai Office of Agricultural Economicsreported that in 2014 herbicides constituted the lar-gest volume of imported pesticides (106,860 tons outof 134,377 tons of pesticides).1 They further reportedthat glyphosate and paraquat were the most com-monly imported herbicides.1 Glyphosate, orN-(phosphonomethyl)glycine, has many tradenames, such as Gallup, Landmaster, Pondmaster,Ranger, Roundup, Rodeo, and Touchdown.2 It is anonselective, systemic, postemergence herbicide thatenters the plant through the leaves and disperses

throughout, inhibiting an enzyme in the shikimatepathway that is essential for the biosynthesis of aro-matic amino acids in plants.3 It has low oral acutetoxicity, with a lethal dose (LD50) of over 4320mg/kgin rats.4 People exposed to glyphosate herbicide candevelop eye and dermal irritation, oral or nasal irri-tation, nausea, headache, or asthma if glyphosate isinhaled.5 Glyphosate was significantly associatedwith an increase of non-Hodgkin’s lymphoma intwo case-control studies.6 Glyphosate was alsofound to be a teratogen in Wistar rats, producingdevelopmental retardation of the fetal skeleton.7

Pregnant women who were exposed to glyphosatebefore conception were found to have an elevated

CONTACT Pornpimol Kongtip pornpimol.kon@mahidol.ac.th Department of Occupational Health and Safety, Faculty of Public Health, MahidolUniversity, Center of Excellence on Environmental Health and Toxicology, Commission on Higher Education, Ministry of Education, 420/1 Rajvithi Road,Rajthavee, Bangkok, 10400, Thailand.

JOURNAL OF AGROMEDICINE2017, VOL. 22, NO. 3, 282–289https://doi.org/10.1080/1059924X.2017.1319315

© 2017 Taylor & Francis

risk of late abortion.8 The US EnvironmentalProtection Agency (EPA) and the InternationalAgency for Research on Cancer (IARC) classifiedglyphosate as probably carcinogenic to humans(Group 2A).9,10

Paraquat (1,1’-Dimethyl-4,4’-bipyridiniumdichloride) is a fast-acting, nonselective herbicide with thecommon trade name of Gramoxone. Paraquat isbanned mainly for health reasons in many countries,such as Sweden, Kuwait, Finland, Austria, Denmark,Slovenia, and Malaysia.11 It destroys the green part ofplants on contact and is often used to eliminate weedsand grasses in agricultural areas and around nonagri-cultural areas such as airports, power and utility sta-tions, and commercial buildings.12,13 Dermal contactis considered the major route of exposure, becauseparaquat is a nonvolatile compound.However, duringspraying operations, droplets are produced that couldbe inhaled.14 Paraquat is a neurotoxicant and has beenassociated with the development of Parkinson’sdisease.15–17 Organochlorine pesticides are also sus-pected to play a role in Parkinson’s disease.18 Bartlettet al.17 showed paraquat uptake in maternal and fetalbrains of rhesus monkeys after the injection of 11C-paraquat during pregnancy.17

Three agricultural areas, Amnatchareon, NakhornSawan, and Karnjanaburi provinces, were selectedfor this study to promote research collaborationwith the three campuses of Mahidol University.The main crops in these provinces are rice, sugar-cane, corn, and vegetables. Most agricultural areas inThailand use more herbicides than other types ofpesticides; however, few data are available aboutagricultural worker exposure to these pesticides,since no screening tests exists in Thailand.However, Amnatcharoen and Nakhorn Sawan pro-vinces have been in the top 10 provinces for pesticidepoisoning cases in the country, usually associatedwith organophosphate and carbamate insecticides.This study is the first to measure glyphosate andparaquat concentrations in maternal and umbilicalcord serums during the normal delivery of pregnantwomen living in three agricultural areas in Thailand.

Materials and methods

Subjects for a pilot birth cohort were recruitedfrom pregnant women who came for prenatalcare at three hospitals in Thailand:

Amnatchareon Hospital in AmnatchareonProvince in the northeast, SawanpracharakHospital in Nakhorn Sawan Province in thelower north, and Paholpolpayuhasena Hospital inKarnjanaburi Province in the west of Thailand,from May to December 2011. To be recruited,the women had to be in their 7th month of preg-nancy, 19–35 years of age, not have diabetes orhypertension, and plan to give birth and havefollow-up infant care at the recruiting hospital. Intotal, 113 pregnant women were interviewed andagreed to participate. Of these 113 women, 81delivered babies in the participating hospitals atfull term with normal labor; 19 delivered at otherhospitals; 3 delivered preterm by cesarean section;9 were full-term cesarean; and 1 full-term deliveryinvolved significant complications and wasdeemed ineligible for follow-up. The 82 subjectsfor this study included 81 full-term normal birthneonate and 1 full-term cesarean birth neonate.

During their 7th month of pregnancy, thewomen were interviewed about their generalhealth, diet, and work exposures, including agri-cultural work, as well as about use of pesticides athome and work. Several questionnaires, each withseveral sections, constituted the data collection.The questionnaire was based on the type of infor-mation collected in previous studies of agriculturalworkers and modified for the conditions of agri-culture and types of pesticide exposures experi-enced in Thailand. The questionnaires werereviewed by staff at each hospital, then pilotedand revised based on comments. One question-naire collected data on demographics and themother’s general health, whereas another collectedbirth data. The pesticide exposure questionnaireconsisted of six sections; the first section contained12 items related to pesticide use in the home oroutside the home, as well as sources of drinkingwater. The second section contained 9 items aboutthe woman’s work history outside the home. Thethird section, with 10 items, covered agriculturalactivities if conducted by the woman. The fourthsection, with 3 items, covered agricultural activitiesconducted by the woman during pregnancy. Thefifth section, with 6 items, asked about the agri-cultural work of family members. The sixth sec-tion, with 30 items, collected detailed informationonly from those who were agricultural workers or

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had family members who were agricultural work-ers and included detailed information on the mix-ing and spraying of pesticides. To summarize, thepesticide exposure questionnaire had 40 items forall subjects and 30 items only for those who wereself-identified as agricultural workers or who hadfamily members who were agricultural workers.For comparisons with agriculturists, women withother occupations were used as the control group.The nurses at the prenatal clinics in the threestudy hospitals were trained to recruit and inter-view subjects. The maternal and umbilical cordserum was collected during delivery by the deliv-ery nurses and was frozen at −45°C until analysis.This study was reviewed and approved by theEthics Committee on Human Rights Related toHuman Experimentation, Mahidol University,and the University of Massachusetts LowellInstitutional Review Board.

Glyphosate and paraquat dichloride wereobtained from Sigma-Aldrich Inc., Singapore.Acetonitrile, trimethylamine, methylene chloride,dichloromethane (all high-performance liquidchromatography [HPLC] grade), and sodiumdodecyl sulfate (SDS) (gas chromatography [GC]grade) were purchased from Apex Chemical,Bangkok, Thailand. Other chemicals were of ana-lytical grade. Analysis was performed with anHPLC system (Agilent 1200 Series) with a fluores-cence detector for glyphosate and ultraviolet (UV)diode array detector for paraquat. For glyphosate,the serum sample was analyzed on Luna 5 μm C18(150 × 4.6 mm) column (Phenomenex, Torrance,CA, USA) with guard column at 45°C. The condi-tion of mobile phase is similar to that of Bernalet al.19 Calibration curves were developed usinghospital serum samples of nonsubjects tested forthe nonpresence of glyphosate and then spikedwith glyphosate to yield final concentrations of12.5, 25, 50, 100, 150, and 200 ng/mL (n = 3replicates). For paraquat, the serum sample wasanalyzed on J’ sphere ODS-H80 column(150 mm × 4.6 mm ID, 4 µm) (YMC Co., Ltd.,Tokyo, Japan) at 35°C using a flow rate of 1.0 mL/min mobile phase and monitored by UV absorp-tion at 256 nm. The mobile phase consisted of 23%acetonitrile and 0.1 M orthophosphoric acid con-taining 300 mg/L of SDS. The mobile phase wasadjusted to pH 3.0 with triethylamine, followed by

filtering with 0.45 µm nylon membrane.Calibration curves were developed using hospitalserum samples of nonsubjects tested for the non-presence of paraquat and then spiked with para-quat to yield final concentrations of 7, 10, 20, 40,60, 80, and 100 ng/mL (n = 3 replicates).

For sample preparation of glyphosate, the serumsample preparation was similar to that of Bernalet al.19 by using 250-µL serum samples, and 30 µLof derivatized glyphosate was injected into theHPLC. The serum sample preparation of paraquatwas performed following the method of Zou et al.20

by using 250-µL serum samples, and 40 µl of thepretreated serum was injected into the HPLC.Evaluation of the detection limit was performedfollowing the National Institute for OccupationalSafety and Health method.21 For determination ofaccuracy and precision, concentrations of hospitalserum samples of nonsubjects tested for the non-presence of the target pesticides were used to pre-pare concentrations of 50, 100, and 150 ng ofglyphosate/mL and 20, 50, and 80 ng of paraquat/mL. Three replicates of each concentration wereanalyzed on three separate days. The calibrationcurves for paraquat and glyphosate were linearover the concentration ranges of 7–100 ng of para-quat/mL serum and 12.5–200 ng glyphosate/mLserum with the correlation coefficient of 0.999 and0.998, respectively. The detection limits for theanalysis of paraquat and glyphosate in serum were0.4 and 0.4 ng/mL, respectively. Values belowdetection limit for both serum glyphosate and para-quat were used as detection limit divided by 2, sincethe data were highly skewed.22 For the glyphosatedetermination method, the recovery of the methodranged from 94.33% to 99.03% with a relative stan-dard deviation (RSD) of <3% for glyphosate con-centrations of 50–150 ng/mL. The recovery of theparaquat determination method ranged from91.78% to 95.15% with an RSD of <4% for paraquatconcentrations of 20, 50, and 80 ng/mL.

The descriptive statistics were calculated usingSPSS (SPSS version 18; PASW Statistics Base 18,Bangkok, Thailand). Since exposures were highlyskewed due to the large percentage of values belowthe limit of detection (LOD), concentrations werereported as the median and range. For comparisonof the paired mother and cord blood serum concen-trations for glyphosate and paraquat, only pairs with

284 P. KONGTIP ET AL.

both measurements above the LOD levels were usedwith the Wilcoxon signed-rank test. Binary logisticregression was used to evaluate whether variousfactors were significantly associated with the prob-ability of having glyphosate or paraquat concentra-tions over the LOD. Several a priori factors wereevaluated for inclusion as potentially significant cov-ariates, such as maternal location/province and edu-cational level of themother, but these were found notto be significantly associated with the probability ofhaving glyphosate or paraquat concentrations overthe LOD. Thus, occupational factors were evaluatedin single-factor models and reported as unadjustedodds ratios (ORs). In models examining secondaryexposure factors, maternal occupation was includedas a covariate in the model to control for the influ-ence of maternal agricultural work on serum levels.

Results

The general characteristics of the 82 pregnant womenwho gave birth during the study are shown in Table 1.The average age was 26 years old (range: 19–34 years),with most having completed secondary school (41%),although 26% only completed primary school. Of the82 women, 39% of the women described their occu-pation as agriculturist/farmer, whereas 21% listedthemselves as a housewife, and about 13% wereemployees or owned their own business (often theseare small retail stands with food or other items forsale). Of the 82 pregnant women who gave birthduring the study, we were only able to collect cord

blood from 75 newborns, all born full term (37–41weeks).

The percentage of maternal samples of glyphosatethat were at or below the LODwas 46.3%, whereas forcord serum 50.7% were ≤LOD (Table 2). For para-quat, 83.3% of the maternal serum samples were≤LOD, whereas 79.7% of the cord serums were≤LOD. Comparison of the glyphosate concentrationsin paired serum samples of mother and cord bloodthat were both >LOD (n = 36) found that they weresignificantly different (P < .001), with the mother’sserum levels the higher of the two. The paraquatconcentrations in paired serum samples of themotherand cord blood that were both >LOD (n = 8) were notsignificantly different (P = .327).

With regard to occupational factors predictingglyphosate exposures, the odds of having a detect-able level of glyphosate in serum were 11.9 higherthan the LOD among women who worked in thefields compared with those who did not. Pregnantwomen who worked in agricultural fields duringthe first, second, or third trimester of pregnancyalso had significantly elevated ORs (13.5, 7.7, and12.4, respectively) of having serum levels >LODcompared with those women who never worked inthe fields. Likewise, pregnant women whoreported picking crops during pregnancy had asignificantly elevated OR (5.4), whereas thosewho reported the agricultural activity of diggingin farm soil or controlling weeds during pregnancydid not have elevated ORs (Table 3).

With regard to secondary factors, pregnant womenwho lived near agricultural fields (<0.5 km) weresignificantly more likely to have serum glyphosatelevels >LOD than those women living far from agri-cultural fields (ORs of 3.7 [crude] and 4.2 [adjustedfor occupation]) (Table 4). Note that there was nosignificant relationship between home location andagricultural occupation (χ2 = 1.01, P = .315); thus,the adjusted OR does not reflect collinearity or con-founding. Those pregnant women who reported afamilymember whowas an agriculturist/farmer livingin the same house were significantly more likely tohave elevated serum glyphosate than those who didnot (OR = 5.9); however, when adjusted for occupa-tion, the OR became nonsignificant, because of thehigh correlation between having a family memberwho was a farmer in the same house and maternaloccupation as a farmer (χ2 = 17.60, P < .001) (Table 4).

Table 1. General characteristics of pregnant women (N = 82).Characteristic n %

Age (years)19–24 35 4525–30 28 3631–34 15 19

Mean ± SD = 25.68 ± 4.33 (Min = 19, Max = 34)Education levelsPrimary school 20 26Secondary school 32 41High school or vocational certificate 17 22Diploma or high vocational certificate 7 9Bachelor degree or upper degree 2 2

OccupationAgriculturist 30 39Employees 3 4Own small business 7 9Housewife 16 21Government officer 1 1Other 20 26

JOURNAL OF AGROMEDICINE 285

With regard to occupational factors predictingparaquat exposures, pregnant women who reporteddigging in farm soil had significantly elevated oddsof having serum paraquat higher than the LOD (OR= 6.0) compared with women who did not (Table 3).Pregnant women who worked in agricultural fieldsduring the third trimester of pregnancy also had asignificantly elevated probability of having a serumparaquat >LOD than those who did not (OR = 5.4).The other risk factors examined did not have a sig-nificant impact on paraquat serum levels of thepregnant women (occupation, controlling weeds, orpicking crops during pregnancy, or working in agri-cultural fields in the first or second trimester)

(Table 3), neither did secondary exposure (homelocation or having a family member who was farmerliving in the home) significantly elevated the risk ofhaving a serum paraquat level >LOD (Table 4).

Discussion

The most striking finding of this study was thatglyphosate concentrations over the LOD were sig-nificantly more likely to be found in the serum ofpregnant women collected at childbirth if theiroccupation was an agriculturist/farmer or con-ducted various agricultural tasks or if they livednear agricultural fields sprayed with pesticides

Table 2. Glyphosate and paraquat levels in maternal and umbilical cord serums.Glyphosate in maternal serum (n = 82) Glyphosate in umbilical cord serum (n = 75)

Concentration (ng/mL) n (%) Concentration (ng/mL) n (%)

≤LOD 38 (46.3) ≤LOD 38 (50.7)1–50 25 (30.5) 1–25 22 (28.3)51–100 10 (12.2) 26–50 9 (12.0)101–150 6 (7.3) 51–75 4 (5.3)151–200 3 (3.7) 76–100 2 (2.7)(Median = 17.5) (Min = 0.2, Max = 189.1) (Median = 0.2) (Min = 0.2, Max = 94.9)

Paraquat in maternal serum (n = 78) Paraquat in umbilical cord serum (n = 69)

Concentration (ng/mL) n (%) Concentration (ng/mL) n (%)

≤LOD 65 (83.3) ≤LOD 55 (79.7)1–20 6 (7.7) 1–20 4 (5.8)21–40 6 (7.7) 21–40 6 (8.7)41–60 1 (1.3) 41–60 4 (5.8)(Median = 0.2)(Min = 0.2, Max = 58.3) (Median =0.2) (Min = 0.2, Max = 47.6)

Table 3. The impact of occupational exposure factors on maternal serum levels using logistic regression for probability of maternalserum concentration >LOD.

Glyphosate Paraquat

Risk factor n OR (95% CI) n OR (95% CI)

Occupation agriculturist 30 11.9 (3.6–39.5)* 26 1.3 (0.4–4.3)Dig in farm soil during pregnancy 14 3.9 (1.0–15.2) 11 6.0 (1.5–24.5)*Control weeds during pregnancy 5 1.2 (0.2–7.9) 5 1.2 (0.1–11.8)Pick crops during pregnancy 17 5.4 (1.4–20.8)* 14 2.4 (0.6–9.3)Work in the field during 1st trimester 19 13.5 (2.8–64.3)* 17 1.8 (0.5–6.8)Work in the field during 2nd trimester 18 7.7 (2.0–29.8)* 16 2.2 (0.6–8.9)Work in the field during 3rd trimester 11 12.4 (1.5–102.7)* 9 5.4 (1.2–24.4)*

*Significant at P < .05.

Table 4. The impact of secondary exposure factors on maternal serum levels using multiple logistic regression for probability ofmaternal serum concentration >LOD.

Glyphosate Paraquat

Risk factor n OR (95% CI) Adjusted OR (95% CI)** n OR (95% CI)

Live near agricultural farmland 40 3.7 (1.5–9.2)* 4.2 (1.4–12.3)* 39 0.8 (0.2–2.6)Family members who work on a farm live in the same house 52 5.9 (2.2–16.1)* 2.8 (0.9–8.7) 47 0.7 (0.2–2.2)

*Significant at P < .05.**Adjusted for maternal occupation as an agriculturist.

286 P. KONGTIP ET AL.

(unspecified), when compared with women whohad no agricultural exposures. Acquavella et al.23

measured glyphosate levels in urine among farm-ers in the United States and found that farmerswho had skin contact with pesticides or did notuse rubber gloves had significantly higher glypho-sate concentrations in their urine.23 Among thosewho did not wear rubber gloves, appreciable dif-ferences were found in the urinary glyphosatelevels between those who repaired equipment dur-ing applications or spilled during mixing/loadingor application. This supports the notion that der-mal contact is an important route of exposure forthis herbicide. Mesnage et al.24 also reported urin-ary glyphosate in one of the children who lived 1.5km away from the farm where their father sprayedglyphosate in France. However, in the US study byAcquavella et al.,23 very few of the spouses (4%)and children (12%) who lived in a home within 1mile of the sprayed farm fields had measureableurinary glyphosate on the day of spraying, and aneven lower percentage had measureable levels ondays 1–3 post application.23 Among the applica-tors, 60% had measureable glyphosate on thespraying day, with a decrease to 27% on the thirdday post application. This raises the question ofthe half-life of glyphosate and how the Thai agri-cultural women giving birth had measureablelevels of glyphosate in their serum. Althoughthese women had regular, repeated exposures toglyphosate, even during their final trimester ofpregnancy, it is unlikely that they were exposedin the field on the day prior to giving birth. It ispossible that these serum levels were caused by thedrift of glyphosate spray, skin contact with thepesticide contaminated family member workingin the fields, contamination of the home throughclothing (take home exposure), or through poorstorage of pesticides near the home.24,25

Alternatively, little is known about the metabolismand storage of pesticides during pregnancy and theimpact on pesticide half-life. The median (range)glyphosate concentrations of maternal and umbi-lical cord serums in this current study were 17.5(0.2–189.1) and 0.2 (0.2–94.9) ng/mL, respectively.The maternal serums of glyphosate at birth weresignificantly higher than those in cord blood ser-ums. It is not known why maternal serum levelswere higher than cord serum samples. At this time,

only one study has looked at serum levels of pes-ticides in pregnant and nonpregnant Canadianwomen who were not agriculturists or living witha spouse who worked with pesticides.26 Theyfound no detectable levels of glyphosate in thepregnant women before birth or in their cordblood samples. However, 5% (2/39) of the non-pregnant women in that study had measureableglyphosate serum levels (including one with alevel of 93.6 ng/mL). Potential exposures in thatstudy were assumed to be through consumption ofpesticides associated with genetically modifiedfoods.26 In our study, we found measureable gly-phosate levels (>LOD) in 14.7% of the maternalserum samples of women who were not agricul-turists/farmers by occupation. This is concerning,because Arbuckle et al.27 studied the effect of gly-phosate exposures on the risk of miscarriageamong women living on farms in Ontario,Canada, and found that women who were exposedto glyphosate before conception (from 3 monthsbefore up to conception) had a higher risk ofspontaneous abortion.27

The 6-fold higher odds of having a paraquat levelin the serum >LOD among the pregnant womenwho reported the agricultural activity of digging infarm soil could be explained by the fact that para-quat degrades slowly under aerobic and anaerobicincubation, and that paraquat has a half-life in soilup to 20 years.11 Therefore, the use of paraquatherbicide in their fields can result in its accumula-tion in the soil and exposures during nonsprayingperiods of agriculture. Exposure to contaminatedsoil through the hands (dermal exposure) couldplausibly lead to higher paraquat concentrationsin serum. Van Wendel De Joode et al. showed thatdermal contact with paraquat was significantlyrelated to paraquat concentration in urine.28

In our study, the paraquat concentration in theserum of pregnant women who were agriculturistsor who participated in growing plants, pickingcrops, or controlling weeds was not differentfrom those who did not engage in these activities.This may be because these women did not useparaquat as an herbicide, but the major source ofparaquat exposure was through eating contami-nated food and vegetables or only through soildisruption activities. Paraquat residues in foods,namely sorghums, olives, potatoes, and maize, as

JOURNAL OF AGROMEDICINE 287

well as cottons and sunflowers, were found afterusing paraquat for crop protection.29 In Thailand,residues of paraquat above the maximum residuelimits for dry soybeans (0.1 mg/kg) were foundafter using paraquat as a preharvest desiccant formung bean seed.30 However, paraquat concentra-tions in many kinds of foods, including corn, rice,cucumber, soybean, fruits, vegetables, meat, milk,and egg, were found to be below the maximumresidue limits recommended by Thailand Ministryof Public Health.31

The median (range) paraquat concentrations ofmaternal and umbilical cord serums in this currentstudy were low: 0.2 (0.2–58.3) and 0.2 (0.2–47.6)ng/mL, respectively, with the majority of samplesbelow the LOD. Maternal serum levels for paraquatwere not different from the paired cord serum levelfor those samples >LOD. We do not have an expla-nation for this, since other case studies have shownparaquat concentrations can cross the placenta, andthat cord blood levels were higher than those inmaternal blood after a paraquat solution wasingested by a pregnant women.32,33

Strength and limitation

This study is the first to measure glyphosate andparaquat concentrations in maternal and cord ser-ums from pregnant women in agricultural areas inThailand. Future work will investigate the relation-ship to neonatal and infant neurobehavioral out-comes. Since the number of samples >LOD waslimited, comparisons between maternal and cordblood levels may not have enough power to seesignificant differences for paraquat. Although thesample size was small (N = 82), significant rela-tionships were found between occupational factorsand both paraquat and glyphosate exposures. Forglyphosate, secondary exposures via living nearfarmlands that spray pesticides was a significantpredictor of glyphosate levels >LOD, even aftercontrolling for maternal occupation as a farmer.

Conclusion

This study suggests that agricultural activities doincrease maternal serum levels of both glyphosateand paraquat, even in samples taken on the day ofbirth. In the case of glyphosate, living near

farmland where pesticides are sprayed can alsosignificantly increase the risk of serum levels>LOD at birth. These results suggest that a studyevaluating the long-term health of childrenexposed to herbicides during gestation should beconsidered. Given that herbicides make up thelargest volume of pesticide imports in Thailand,and that imports continue to increase, furtherregulation of the sale and use of pesticides mayhelp safeguard the health of Thai children.

Acknowledgments

The authors would like to thank the nurses, doctors, andpatients who participated in the study, includingPaholpolphayuhasena, Sawanpracharuk, and Amnatcharoenhospitals in Kanchanaburi, Nakhorn Sawan, andAmnatcharoen provinces, respectively, for their help, sup-port, and care.

References

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2. Monsanto. Backgrounder: history of Monsanto’s gly-phosate herbicides. Available at: http://www.monsanto.com/products/documents/glyphosate-background-materials/back_history.pdf. Published 2005. AccessedJanuary 21, 2015.

3. McQueen H, Callan AC, Hinwood AL. Estimatingmaternal and prenatal exposure to glyphosate in thecommunity setting. Int J Hyg Environ Health.2012;215:570–576.

4. Pesticide Action Network UK. Glyphosate fact sheet.Available at: http://www.pan-uk.org/pestnews/Actives/glyphosa.htm. Published 1996. Accessed January 15, 2016.

5. Williams GM, Kroes R, Munro IC. Safety evaluationand risk assessment of the herbicide Roundup and itsactive ingredient, glyphosate, for humans. RegulToxicol Pharmacol. 2000;31:117–165

6. Hardell L, Eriksson M, Nordstrom M. Exposure topesticides as risk factor for non-Hodgkin’s lymphomaand hairy cell leukemia: pooled analysis of two Swedishcase-control studies. Leuk Lymphoma. 2002;43:1043–1049.

7. Dallegrave E, Mantese FD, Coelho RS, Pereira JD,Dalsenter PR, Langeloh A. The teratogenic potentialof the herbicide glyphosate—roundup in Wistar rats.Toxicol Lett. 2003;142:45–52.

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