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5 Epidemiologic Studies: Compendium of New Publications and Background on Multiple Referenced Populations The continuing effort to evaluate and integrate epidemiologic studies pertinent to possible health effects of the chemicals of interest—2,4-dichlorophenoxyacetic acid (2,4-D), 2,4,5-trichlorophenoxyacetic acid (2,4,5-T) and its contaminant 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 4-amino-3,5,6-trichloropicolinic acid (picloram), and cacodylic acid (dimethyl arsenic acid or DMA)—has in - volved the review of thousands of publications over successive updates, Veterans and Agent Orange: Health Effects of Herbicides Used in Vietnam, hereafter re- ferred to as VAO (IOM, 1994), Veterans and Agent Orange: Update 1996 (IOM, 1996), Update 1998 (IOM, 1999), Update 2000 (IOM, 2001), Update 2002 (IOM, 2003a), Update 2004 (IOM, 2005), Update 2006 (IOM, 2007), and Up- date 2008 (IOM, 2009), and three shorter more focused VAO reports: Herbicide/ Dioxin Exposure and Type 2 Diabetes, hereafter referred to as Type 2 Diabetes (IOM, 2000), Herbicide/Dioxin Exposure and Acute Myelogenous Leukemia in the Children of Vietnam Veterans, hereafter referred to as Acute Myelogenous Leukemia (IOM, 2002), and Length of Presumptive Period for Association Be- tween Exposure and Respiratory Cancer, hereafter referred to as Respiratory Cancer (IOM, 2004). The first part of this chapter tabulates epidemiologic publications that ap - peared in the period from October 1, 2008 (the closing date for inclusion in Update 2008 [IOM, 2009]), through September 30, 2010, as a compendium of new information on human health outcomes considered by the present committee. In this chapter and later chapters, epidemiologic studies are organized into three categories according to the populations being studied: Vietnam veterans, occupa - tional populations other than Vietnam veterans, and nonoccupational populations affected by environmental exposures. Within each population, various study de - 120
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121 EPIDEMIOLOGIC STUDIES signs (most important, cohort, case–control, and cross-sectional) have strengths and weaknesses (see Chapter 2) that influence their potential to contribute evi - dence considered in the health-outcomes chapters. The second part of this chapter provides design information on populations that are the subjects of multiple references in this and earlier VAO reviews, in - cluding new studies of populations that have been studied previously and studies of new populations with multiple health outcomes, to avoid repeating design information in multiple health-outcomes chapters. (The design information on studies of new populations that involve single health outcomes is provided in the various health-outcomes chapters.) For presentation of the background informa - tion, the study populations are arranged into the categories based on whether they are composed of Vietnam veterans, occupationally exposed workers, or en- vironmentally exposed individuals or were assembled according to a case–control approach focused on particular health outcomes. In addition to reviewing studies involving exposures to the specific chemi- cals of interest listed previously, this and earlier VAO committees have also considered studies that examined compounds chemically related to the herbi - cides used in Vietnam, such as 2-(2-methyl-4-chlorophenoxy) propionic acid, hexachlorophene, and chlorophenols, particularly 2,4,5-trichlorophenol. Some publications did not indicate the specific herbicides to which study participants were exposed or the magnitude of exposure; those limitations were considered when the committee weighed the relevance of each publication, as detailed in Chapter 2. The committee also considers studies of exposure to polychlorinated biphenyls (PCBs) and other dioxin-like compounds (DLCs) informative if their results were reported in terms of TCDD toxic equivalents (TEQs) or concentra - tions of specific congeners of DLCs. Available details of exposure assessment and use of the resulting data in analyses are discussed in Chapter 3, which follows the same sequence to categorize study populations. NEW EPIDEMIOLOGIC PUBLICATIONS The new epidemiologic publications reviewed by the committee for this update are listed in Tables 5-1, 5-2, and 5-3. The conditions listed in the “Health Outcomes reported” column are indicative of the chapters in which the new publications are considered. Note, however, that studies assessing the occurrence of various cancers following exposure scenarios temporally comparable to expo - sure during military service are discussed in Chapter 7, which addresses cancer outcomes in the veterans themselves. Studies of childhood cancers in relation to parental exposure to the chemicals of interest are discussed in Chapter 8, which addresses possible adverse effects in the veterans’ offspring. Cancer studies that consider only childhood exposure are not considered relevant to the committee’s charge.
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122 VETERANS AND AGENT ORANGE: UPDATE 2010 TABLE 5-1 Publications Reporting a Single Health Outcome in New Populations Exposure Measure(s) Health Outcome Author Study Design Having Results Reported Study Population Studies of Vietnam Veterans Shah Case–control Reported as Progression of Veterans with radical et al., “previous prostate cancer prostatectomies examined at 1 2009 agent orange of 5 VA Healthcare facilities; exposure” health data culled from the SEARCH database Occupational Studies Individuals, ≥ 50 yrs of age, Dhillon Case–control Occupational PD et al., and diagnosed with PD and living 2008 environmental in eastern TX exposures, including 2.4-D, 2,4,5-T, Silvex Elbaz Case–control Herbicides, PD PD patients (18–75 yrs of et al., phenoxys age) who applied for free 2009 healthcare for agriculture workers or related occupations in France Lo et al., Case–control Herbicides Colorectal Egyptian cases and hospital- 2010 (unspecified) carcinoma matched controls Tanner Case–control 2,4-D PD Consecutively eligible PD et al., patients recruited from 8 US 2009 movement disorder clinic Environmental Studies Aronson Case–control POPs (dl PCBs Prostate cancer Male clinic patients (50–80 et al., 118 and 156) in yrs of age) who visited 1 of 5 2010 serum urologists from 1997 through 1999 in Kingston, Ontario Chang Cross-sectional TEQs Type 2 diabetes Residents living near a et al., (insulin deserted PCP factory in Tainan 2010 resistance and City, Taiwan pancreatic β-cell function Cok Case–control Organochlorine Infertility Adipose taken from fertile and et al., pesticides and infertile men during surgical 2010 PCB (including procedures in Turkey dl-PCB 118) in adipose tissue
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123 EPIDEMIOLOGIC STUDIES TABLE 5-1 Continued Exposure Measure(s) Health Outcome Author Study Design Having Results Reported Study Population Cornelis Case–control Herbicides— Bladder cancer Application of GIS to et al., undefined agricultural pesticide use to a 2009 bladder cancer study Dai and Ecologic Dioxin levels in Breast cancer Breast cancer incidence Oyana, soil (ppt–TEQ) and residential proximity to 2008 dioxin-contaminated areas (GIS study) Dallaire Cross-sectional Dl PCBs Thyroid Random sample of Inuit et al., (including PCB function population of Québec, Canada 2009 105, 118, 156, ~170, ~180) Darnerud Case–control TEQs for dioxin/ Thyroid Swedish mother–child pairs et al., furans and hormone levels (1996–1999); analysis of 2010 mono-ortho breast milk maternal pre-birth PCBs serum, and child’s serum Dhooge Cross-sectional Dl PCB 118 in BMI Random sampling of Flemish et al., serum adults (50–65 yrs of age) and 2010 adolescents residing in study area Farooq Case–control Pesticide use for Breast cancer Self-reported residential et al., “weeds” pesticide use in and around 2010 New York City, NY Giordano Case–control Serum levels of Hypospadias Hypospadic children and et al., dl PCB 118 and controls recruited from 2 2010 non-dl PCBs hospitals in Rome, Italy (September 2005–May 2007) Hodgson Cohort TEQs for PCBs Bone mineral Baltic adults (60–81 yrs of et al., (including dl density age) 2008 PCBs 105, 118, 156, 157, 167) Konishi Prospective Dioxins, furans, Birth weight Pregnant women recruited et al., cohort dl PCBs, TEQ (July 2002–October 2005) in 2009 (1998 and 2006) Sapporo, Japan in maternal serum Krüger Cohort Dioxin-like Chromosome European and inuit men; et al., serum activity of activity in subset of INUENDO study 2008 lipophilic POPs sperm continued
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124 VETERANS AND AGENT ORANGE: UPDATE 2010 TABLE 5-1 Continued Exposure Measure(s) Health Outcome Author Study Design Having Results Reported Study Population Kuscu Ecologic TEQ in soil MIH Elementary school children et al., from industrialized and 2009 nonindustrialized areas in Turkey Laisi Case–control PCDD/F and MIH Mothers and children with et al., PCB TEQs in cleft palates born 1995–1999 2008 breast milk and control children in Finland Maluf Case–control Herbicides AA LATIN case–control study; et al., or pesticides compared exposures for the 2009 (agricultural or previous 30–365 days for AA home use) patients and controls Niskar Case–control Serum level Endometriosis Patients at a reproductive et al., congeners of medicine clinic in Atlanta, GA 2009 dioxin, furans, and PCBs Porpora Case–control Serum TEQs Endometriosis Italian women undergoing et al., laparoscopy for endometriosis 2009 or other benign gynecologic condition Rull Case–control Chlorinated ALL Northern California Childhood et al., phenol— Leukemia Study—Residential 2009 including 2,4-D, proximity (within a half-mile) MCPA, MCPP, of pesticide application diclofop-methyl Shim Case–control Residential or Childhood Atlantic Coast Childhood et al., occupational brain cancer Brain Cancer Study; maternal 2009 exposure to (astrocytomas report of parental pesticide herbicides and primitive exposure in 2 yrs prior to birth neuroectodermal tumors) Tawara Cohort TEQs (TCDD Birth size Mother-infant pairs from et al., and other dl- Hokuriku District, Japan (an 2009 congeners, total area with high coastal fish TEQ) consumption) Turyk Cross-sectional POPs (including Diabetes Great Lakes sport-fish et al., dl-PCBs 118, consumers 2009 167)
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125 EPIDEMIOLOGIC STUDIES TABLE 5-1 Continued Exposure Measure(s) Health Outcome Author Study Design Having Results Reported Study Population Verhulst Prospective Gestational BMI (first 3 yrs Mother-infant pairs recruited et al., birth cohort exposure; cord of life) from maternity wards 2009 blood levels of throughout Flanders, Belgium PCBs, including (September 2002–February dl 118 2004) Vidal Case–control Herbicide use Progressive In or outpatients from 5 large et al., for gardening supranuclear Parkinson disorder centers in 2009 palsy (a France Parkinsonian syndrome) Vlajinac Case–control Herbicides PD Newly diagnosed PD patients et al., in Belgrade, Serbia (January 2010 2001–November 2005) Waller Case–control 2,4-D Gastroschisis Live-born singleton infants et al., (abdominal with gastroschisis identified 2010 hernia) from Washington State birth certificates and US Geological Survey databases Ward Case-control Residential ALL Northern CA Childhood et al., carpet dust Leukemia Study; analysis ALL 2009 (including dl- and contents of residential PCBs 105, 118, carpet dust 170, 180) Zhang Case–control TEQs from cord Thyroid Electronic-waste recycling et al., blood hormone community in China 2010 homeostasis Zota Case–control Pesticide use Breast cancer Cape Cod Breast Cancer and et al., for “lawn care” Environment Study—use of 2010 or “indoor or household cleaners by Cape outdoor plant Cod residents care” ABBREVIATIONS: 2,4-D, 2,4-dichlorophenoxyacetic acid; 2,4,5-T, 2,4,5-trichlorophenoxyacetic acid; AA, aplastic anemia; AHR, aryl hydrocarbon receptor; ALL, acute lymphocyte leukema; BMI, body mass index; dl, dioxin-like; GIS, geographic information system; MCPA, 2-methyl-4-chloro - phenoxyacetic acid; MIH, molar incisor hypomineralization; PCB, polychlorinated biphenyl; PCDD, polychlorinated dibenzo-p-dioxin; PCDF, polychlorinated dibenzofuran; PD, Parkinson disease; PE, peritoneal endometriosis; POP, persistent organic pollutants; SEARCH, Shared Equal Access Research Cancer Hospital; TCDD, 2,3,7,8-tetrachlorodibenzo-p-dioxin; TEQ, (total) toxic equivalent; VA, Department of Veterans Affairs.
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126 VETERANS AND AGENT ORANGE: UPDATE 2010 TABLE 5-2 Publications on Multiple Health Outcomes in New Study Populations Exposure Study Measures(s) Health Outcome(s) Author Design Having Results Reported Study Population Occupational Studies Orsi et al., Case–control Pesticides, HL, NHL, MM, French, male patients 2009 herbicides lymphoproliferative with lymphoid (phenoxys) syndrome (including neoplasms (18–75 yrs CLL, hairy cell leukemia) of age) and matched controls Environmental Studies Halldorsson Cohort dl activity in Birth weight and Danish National et al., 2009 maternal serum development at 6 months Birth Cohort; women (25–35 yrs of age) chosen according to their intake of fatty fish ABBREVIATIONS: CLL, chronic lymphocytic leukemia; dl, dioxin-like; HL, Hodgkin lymphoma; NHL, non-Hodgkin lymphoma; MM, multiple myeloma. Publications Reporting a Single Health Outcome in New Populations New publications reporting a single health outcome in populations not stud - ied previously are listed in Table 5-1 with an indication of the outcomes. Descrip- tions and critiques of the designs of these studies are provided in the sections of the report that discuss the results on the particular health outcomes. Publications Reporting Multiple Health Outcomes in New Populations New publications reporting multiple health outcomes in populations not studied previously are listed in Table 5-2, with a list of outcomes that were inves- tigated. Comprehensive discussions of the designs of these studies are presented in the second part of this chapter, organized according to the type of study popula- tion. The results, with comments related to their reliability or limitations, appear in the appropriate outcome-specific sections of Chapters 6–11. New Publications on Previously Studied Populations A number of long-term studies of populations exposed to the chemicals of interest are of particular importance to the VAO project. The disease experiences of those populations are updated with the passage of time. Placing each new publication in its historical context helps the committee to combine the evidence
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127 EPIDEMIOLOGIC STUDIES TABLE 5-3 Publications on Previously Studied Populations Exposure Measure(s) Having Health Outcome(s) Author Study Design Results Reported Study Population Studies of Vietnam Veterans Cypel and Kang, Retrospective Service in Vietnam Mortality through ACC veterans 2010 cohort during Vietnam 2005 from all who handled/ War causes; all cancers; sprayed herbicides cancers (oral/ in Vietnam vs pharynx, digestive, non-Vietnam respiratory, prostate, veteran peers or testicular, skin, US men brain, lymphopoietic [leukemia]), diabetes, circulatory (HT, cerebrovascular), respiratory (pneumonia, influenza, COPD), digestive (cirrhosis of liver) O’Toole et al., Longitudinal Service in Vietnam Prevalence Interviewed 2009 cohort during Vietnam of neoplasms sample of War (melanoma, Australian prostate), thyroid, Vietnam veterans diabetes, lipids, vs results of eye, ear, circulatory general population (HT, IHD, on National cerebrovascular), Health Survey respiratory disorders, digestive disorders, RA (also much investigation of PTSD and other psych problems) Occupational Studies Andreotti et al., Cohort 2,4-D Pancreatic cancer AHS (private 2009 and commercial applicators and spouses) continued
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128 VETERANS AND AGENT ORANGE: UPDATE 2010 TABLE 5-3 Continued Exposure Measure(s) Having Health Outcome(s) Author Study Design Results Reported Study Population Boers et al., 2010 Cohort Chlorophenoxy Follow-up mortality Subcohort of herbicides (1955–2006) from IARC cohort stomach, pancreas, (Netherlands) lung, prostate, bladder, and kidney cancers; melanoma, NHL, leukemia, endocrine/blood diseases, nervous system, IHD, other heart disease, cerebrovascular, respiratory diseases, digestive diseases, (genitourinary diseases) Collins et al., Cohort TCDD, PCP, Mortality from Subcohort of 2009a,b PCDD, 2,4,5-T cancers—all and NIOSH (Dow specific, diabetes, Chemical, cerebrovascular, Midland, IHC, respiratory Michigan plant disorders, digestive workers) disorders Crawford et al., Cohort Herbicides, Hearing loss AHS (licensed 2008 including 2,4-D, pesticide 2,4,5-T, 2,4,5-TP applicators) Dennis et al., Cohort Herbicides, Melanoma AHS (licensed, 2010 including 2,4-D, male pesticide 2,4,5-T, 2,4,5-TP applicators) Firestone et al., Case–control 2,4-D occupational PD Expansion of 2010 exposure Firestone et al. (2005) adding cases newly diagnosed 2003–2006 to those diagnosed 1992–2002 at University of Washington
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129 EPIDEMIOLOGIC STUDIES TABLE 5-3 Continued Exposure Measure(s) Having Health Outcome(s) Author Study Design Results Reported Study Population Goldner et al., Cohort 2,4-D, 2,4,5-T Thyroid disease AHS (female 2010 spouses of private applicators) Hoppin et al., Cohort 2,4-D, 2,4,5- Adult-onset asthma AHS and 2009 T, 2,4,5-TCP, Agricultural dicamba Cohort Consortium Landgren et al., Cohort 2,4-D, dicamba MGUS AHS (licensed, 2009 male pesticide applicators) McBride et al., Cohort 2,4,5-T, phenoxy Mortality Subcohort of 2009a,b herbicides, (cancers—all and IARC cohort picloram specific, diabetes, (New Zealand) cardiovascular disease, respiratory disorders) Mills et al., 2009 Cohort 2,4-D, 2,4,5-T, Myocardial AHS (licensed, 2,4,5-T infarction (mortality male pesticide and incidence) and applicators) long-term pesticide use Pelclová et al., Cohort 2,4,5-T Neurological status, Czech 2,4,5-T 2009 arterial plaques, workers—40 yr diabetes, lipids, HT, follow-up IHD Slager et al., Cohort 2,4-D Rhinitis AHS (commercial 2009 pesticide applicators [male and female]) Environmental Studies Colt et al., 2009 Case–control TEQs, ndl PCB NHL NCI–SEER 180, α-chlordane Study—newly in serum or dust diagnosed NHL patients (20 to 74 yrs of age) at 4 SEER registries continued
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130 VETERANS AND AGENT ORANGE: UPDATE 2010 TABLE 5-3 Continued Exposure Measure(s) Having Health Outcome(s) Author Study Design Results Reported Study Population Cordier et al., Cohort Emissions from Urinary tract birth Rhone-Apes, 2010 municipal solid defects France residents waste living near waste incinerators incinerator Eskenazi et al., Cohort Serum Time to pregnancy SWHS (20 yr 2010 concentrations of follow-up in TCDD Seveso women 0–40 yrs of age at time of the accident) Ha et al., 2009 Cross- Dioxins, furans, dl Newly diagnosed NHANES sectional PCBs HT (1999–2002) Lee et al., 2008 Cross- Serum PN NHANES sectional concentrations of (1999–2002) PCDDs, PCDFs, dl and non-dl PCBs, including dl PCBs 74, 118, 126, 156, 169 McDuffie et al., Case–control “pesticides” in HL, NHL, MM, Cross-Canada 2009 article; listed in STS Study of Update 2002 as Pesticides and phenoxyherbicides, Health 2,4-D, and Mecoprop Ng et al., 2010 Case–control Organochlorines NHL Canadian (including dl PCBs NHL patients 105, 118, 156) (20–70 yrs of age); follow-on to Spinelli et al., 2007 Pesatori et al., Case–control Serum Incidence cases of Seveso population 2008 concentrations of pituatary adenomas (1976–1996); TCDD incidence cases identified by hospital discharge records
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229 EPIDEMIOLOGIC STUDIES Pearce NE, Smith AH, Howard JK, Sheppard RA, Giles HJ, Teague CA. 1986b. Non-Hodgkin’s lymphoma and exposure to phenoxyherbicides, chlorophenols, fencing work, and meat works employment: A case–control study. British Journal of Industrial Medicine 43:75–83. Pearce NE, Sheppard RA, Smith AH, Teague CA. 1987. Non-Hodgkin’s lymphoma and farming: An expanded case–control study. International Journal of Cancer 39:155–161. Pelclová D, Fenclová Z, Dlasková Z, Urban P, Lukáš E, Procházka B, Rappe C. 2001. Biochemical, neuropsychological, and neurological abnormalities following 2,3,7,8-tetrachlorodibenzo-p- dioxin (TCDD) exposure. Archives of Environmental Health 56:493–500. Pelclová D, Fenclová Z, Preiss J, Procházka B, Spácil J, Dubská Z, Okrouhlík B, Lukáš E, Urban P. 2002. Lipid metabolism and neuropsychological follow-up study of workers exposed to 2,3,7,8- tetrachlorodibenzo-p-dioxin. International Archives of Occupational and Environmental Health 75(Suppl l):S60–S66. Pelclová D, Prazny M, Skrha J, Fenclová Z, Kalousova M, Urban P, Navratil T, Senholdova Z, Smerhovsky Z. 2007. 2,3,7,8-TCDD exposure, endothelial dysfunction and impaired micro- vascular reactivity. Human and Experimental Toxicology 26(9):705–713. Pelclová D, Fenclova Z, Urban P, Ridzon P, Preiss J, Kupka K, Malik J, Dubska Z, Navratil T. 2009. Chronic health impairment due to 2,3,7,8-tetrachloro-dibenzo- p-dioxin exposure. Neuroendo- crinology Letters 30(Suppl 1):219–224. Peper M, Klett M, Frentzel-Beyme R, Heller WD. 1993. Neuropsychological effects of chronic expo - sure to environmental dioxins and furans. Environmental Research 60:124–135. Persson B, Dahlander A-M, Fredriksson M, Brage HN, Ohlson C-G, Axelson O. 1989. Malignant lymphomas and occupational exposures. British Journal of Industrial Medicine 46:516–520. Persson B, Fredriksson M, Olsen K, Boeryd B, Axelson O. 1993. Some occupational exposures as risk factors for malignant lymphomas. Cancer 72:1773–1778. Pesatori AC, Consonni D, Tironi A, Landi MT, Zocchetti C, Bertazzi PA. 1992. Cancer morbidity in the Seveso area, 1976–1986. Chemosphere 25:209–212. Pesatori AC, Consonni D, Tironi A, Zocchetti C, Fini A, Bertazzi PA. 1993. Cancer in a young popu - lation in a dioxin-contaminated area. International Journal of Epidemiology 22:1010–1013. Pesatori AC, Zocchetti C, Guercilena S, Consonni D, Turrini D, Bertazzi PA. 1998. Dioxin exposure and nonmalignant health effects: A mortality study. Occupational and Environmental Medicine 55(2):126–131. Pesatori AC, Baccarelli A, Consonni D, Lania A, Beck-Peccoz P, Bertazzi PA, Spada A. 2008. Aryl hydrocarbon receptor-interacting protein and pituitary adenomas: A population-based study on subjects exposed to dioxin after the Seveso, Italy, accident. European Journal of Endocrinology 159(6):699–703. Pesatori AC, Consonni D, Rubagotti M, Grillo P, Bertazzi PA. 2009. Cancer incidence in the popula - tion exposed to dioxin after the “Seveso accident”: Twenty years of follow-up. Environmental Health 8:1 of 11. Petreas M, Smith D, Hurley S, Jeffrey SS, Gilliss D, Reynolds P. 2004. Distribution of persistent, lipid-soluble chemicals in breast and abdominal adipose tissues: Lessons learned from a breast cancer study. Cancer Epidemiology, Biomarkers and Prevention 13(3):416–424. Phuong NTN, Huong LTD. 1983. The effects of toxic chemicals on the pregnancy of the women living at two localities in the South of Vietnam. Summarized in: Constable JD, Hatch MC. Reproduc- tive Effects of Herbicide Exposure in Vietnam: Recent Studies by the Vietnamese and Others. As cited in Constable and Hatch, 1985. Phuong NTN, Thuy TT, Phuong PK. 1989a. An estimate of differences among women giving birth to deformed babies and among those with hydatidiform mole seen at the Ob-Gyn hospital of Ho Chi Minh City in the south of Vietnam. Chemosphere 18:801–803. Phuong NTN, Thuy TT, Phuong PK. 1989b. An estimate of reproductive abnormalities in women in - habiting herbicide sprayed and non-herbicide sprayed areas in the south of Vietnam, 1952–1981. Chemosphere 18:843–846.
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