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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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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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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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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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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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