Neurobehavioral Performance of Adult and
Adolescent Agricultural Workers
Diane S. Rohlmana,*, Michael Lasareva, W. Kent Angera,
Jennifer Scherera, Jeffrey Stupfela, Linda McCauleyb
aCenter for Research on Occupational and Environmental Toxicology (CROET), L606,
Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239, USA
bUniversity of Pennsylvania, Philadelphia, PA 19104, USA
Received 21 October 2005; accepted 30 October 2006
Available online 4 December 2006
There are many occupational hazards associated with working in agriculture including risk of injury and exposure to pesticides. Research
examining neurobehavioral effects of pesticide exposure have focused primarily on the acute effects in adults working in agriculture.
Organophosphate poisoned populations have shown a consistent pattern of deficits when compared to a non-exposed or non-poisoned population
on measures of motor speed and coordination, sustained attention, and information processing speed. Fewer studies have examined the effect of
long-term low-level exposure on nervous system functioning in agricultural workers. Pesticides are thought to pose a considerably higher risk to
children than to adults, yet little is known about the extent or magnitude of health problems related to occupational exposure to pesticides in
children and adolescents. The present study compared the neurobehavioral performance of adolescents and adults working in agriculture and
examined the impact of years working in agriculture on neurobehavioral performance. One hundred seventy-five Hispanic adolescent and adults
completed a neurobehavioral test battery consisting of 10 computer-based tests measuring attention, response speed, coordination and memory.
Age, gender, school experience, and years working in agriculture all impacted performance on the neurobehavioral tests. Comparison of adult and
adolescents did not reveal decreased neurobehavioral performance in adolescents. On several tests the adolescents performed better than adult
These findings suggest that, at the time of exposure to pesticides, adolescents are not more vulnerable to the effects of working in agriculture.
Evidence from this study suggests that cumulative exposure to low levels of pesticides over many years of agricultural work is associated with
neurological impairment as measured by the Selective Attention, Symbol-Digit, Reaction Time tests. Experience handling pesticides was also
associated with deficits in neurobehavioral performance.
# 2006 Elsevier Inc. All rights reserved.
Keywords: Neurobehavioral tests; Pesticides; Adolescents; Agriculture; Hispanic
Agricultural work has one of the highest injury rates in the
workplace (Arcury and Quandt, 1998a,b). Compounding this
problem, agricultural or farm workers are a high-risk group for
exposure to chemicals, including pesticides, used in agricul-
ture. Exposure to pesticides has been linked with chronic and
acute health effects (Woodruff et al., 1994). Workers come in
contact with pesticides through occupational exposure as well
as drift from living in housing located near the fields
(Loewenherz et al., 1997). Exposure may also occur when
pesticides are brought into the home on workers clothing and
skin. Because the majority of fruits and vegetables produced in
the United States are harvested by hand (Oliveira et al., 1993),
exposures may occur during the application of the pesticides or
during the cultivation or harvesting of the crop.
Themajorityofseasonal andmigrant agriculturalworkersin
the United States are Hispanic (Mines et al., 1997). Agriculture
workers range in age from children in their teens to adults in
their 60s (Arcury and Quandt, 1998a,b). Adolescents working
NeuroToxicology 28 (2007) 374–380
* Corresponding author. Tel.: +1 503 494 2513; fax: +1 503 494 4278.
E-mail address: email@example.com (D.S. Rohlman).
0161-813X/$ – see front matter # 2006 Elsevier Inc. All rights reserved.
in agriculture can either be children of seasonal or migrant
farmworkers or local youth living in agricultural communities.
A third group consists of adolescents who migrate and travel
independently from their families. These emancipated minors
tend to be young men from Mexico (Gabbard et al., 1999).
Adolescent farmworkers have other needs that make them
unique from the general farmworker population, including the
fact that many are new immigrants to the US and working in
agriculture for the first time. Also emancipated minors may be
living on their own without adult supervision.
In recent years there has been heightened concern over the
potential of occupational or environmental exposures to affect
neurological function in children and adolescents. Adolescents
who work in agriculture are vulnerable to the same risks of
exposures as adult workers. Pesticides are thought to pose a
considerably higher risk to children due to behavior (e.g.,
increased hand-to-mouth activity) and potentially longer-term
exposure over a working lifetime, overall higher activity levels
and faster metabolism, and smaller body weight per exposure
(Meister, 1991). There is also concern about the impact of
neurotoxicants on the developing central nervous system
(Amler and Gibertini, 1996). During adolescence there are
significant anatomical and maturational changes in the brain
(Andersen, 2003; Brown et al., 2000; Spear, 2002). However,
very little research has examined the impact of neurotoxicants
on the central nervous system of adolescents (Adams et al.,
2000; Brown et al., 2000; Spear, 2002).
Adolescents are engaged in similar agricultural work tasks
as adult workers. Studies of adolescent farmworkers in Oregon
applying pesticides (McCauley et al., 2004, 2002). Further,
littleisknownaboutthe extentormagnitude ofhealth problems
related to occupational exposure to pesticides in children and
adolescents. Environmental exposures and health effects in
children have been poorly characterized. Even less scientific
evidence is available to identify adverse effects of pesticide
exposure in children as a basis for risk assessment.
1.1. Pesticides and neurobehavioral performance
Deficits on measures of motor speed and coordination,
including latency and response speed measures, have been
reported in organophosphate (OP) pesticide poisoned adult
populations tested after recovery (Reidy et al., 1992; Rosen-
stock et al., 1991; Savage et al., 1988; Steenland et al., 1994)
and in different occupational workers chronically exposed to
pesticides (Bazylewicz-Walczak et al., 1999; Kamel et al.,
2003; Rohlman et al., 2001a,b; Rolda ´n-Tapia et al., 2005;
Stephens et al., 1995). A broad range of deficits (including
visual motor speed, verbal abstraction, attention, and memory)
was found in adult cotton pesticide applicators in Egypt
(Farahat et al., 2003).
There is little research on the effects of OP pesticides on
children. Using versions of some of the same tests employed in
cognitive functioning and reaction time in adolescents aged 13–
18 working in agriculture as compared to adolescents not
working in agriculture. Measuring growth and development,
differences in preschool children presumably exposed to
pesticides were found when compared to children less-exposed
(Guillette et al., 1998). Although there were no differences in
growth patterns, the exposed children showed deficits in hand-
eye coordination, memory and ability to draw a person.
Preschool children whose parents were currently working in
agriculturehad significantlypoorerperformanceonmeasures of
response speed and latency than children with parents not
working in agriculture (Rohlman et al., 2005). School-age
children in Ecuador whose mother’s were occupationally
exposed to pesticides during pregnancy had increased blood
pressure and reduced performance on a visuospatial task, a
copying task, compared to controls (Grandjean et al., 2006). In
addition urinary metabolites, reflecting a current measure of
A study comparing health effects, biomarkers of exposure,
and neurobehavioral performance between Hispanic adoles-
cents and adults currently working in agriculture and
adolescents and adults not currently working in agriculture
was conducted. In this paper we present the results of the
comparison of neurobehavioral performance among the
different study populations and the influence of age, gender,
school experience and years working in agriculture on test
performance. The impact of self-reported pesticide use on
neurobehavioral performance was also reported.
During the summer of 2004, 119 Hispanic adults and
adolescents currently working in agriculture (AG) and 56
Hispanic adolescents and adults not currently working in
agriculture (non-AG) completed the neurobehavioral test
battery. Participants were recruited from Hispanic communities
in Oregon through ESL (English as a Second Language)
classes, labor camps, and Migrant Education programs.
Farmworker participants were currently working as field
workers and comparison groups had not worked in the farm
fields for at least 1 year, but may have had a history of
agricultural work. People working in landscaping or plant
nurseries were excluded from the study. An adolescent was
defined as an individual between 12 and 18 years of age. An
adult was defined as an individual between 19 and 60 years of
The majority of participants were immigrants from Mexico,
primarily from the state of Oaxaca. Nine participants were born
in the United States. Sixty-seven participants listed an
indigenous dialect as their primary language. Participants
were excluded from the study if they did not speak Spanish or
Participants completed a Spanish-language consent form
that was explained to the participants. Participants then
D.S. Rohlman et al./NeuroToxicology 28 (2007) 374–380375
completed tests from a neurobehavioral test battery and an
interview with an Examiner fluent in Spanish and English.
Biological samples for analysis of biomarkers of exposure to
pesticides and DNA damage were also collected and analysis is
currently in progress and not the focus of this paper. The
interview was administered one-on-one and consisted of
questions regarding demographic information, health, work
practices and home hygiene questions. The neurobehavioral
test battery was administered to each participant on a computer.
Between six and eight participants were working at any time,
with an examiner fluent in Spanish and English present to
2.3. Neurobehavioral battery
The Behavioral Assessment and Research System (BARS)
was developed for use with a broad range of working
populations having varied education levels and cultural
backgrounds (Anger et al., 1996; Rohlman et al., 2003),
including children (Rohlman et al., 2000, 2001a,b). Features of
the BARS that enable this broad application include: simple
language instructions broken down into basic concepts (step-
by-step training with competency testing at each instruction
step); a ‘‘smiling face’’ used to reinforce performance; and
adjustable parameter settings (Rohlman et al., 1996). A durable
response unit with nine response buttons is placed over a
keyboard (Rohlman et al., 2003) to minimize the impact of
working on a potentially intimidating device such as a
computer keyboard. The BARS tests presented in Table 1
were selected, based on previous evidence of effects of
pesticides on the functions tested (Rohlman et al., 2000,
2.4. Statistical analysis
Neurobehavioral performance measures and demographic
variables such as age and education were summarized using
means and standard deviations; dichotomous or discrete multi-
level data were summarized with proportions. Multiple
regression was applied separately to each neurobehavioral test
measure to assess the effect of years working in agriculture
(greater years assumed to produce worse performance). One-
sided p-values were used to test the hypothesis that adolescents
working in agricultural would have decreased neurobehavioral
performance when compared to their adult counterparts. The
continuous covariates of age, years of education in the
participant’s country of origin, and years spent working in
agriculture were entered into the models assessing the
differences in adolescent and adult farmworkers. Gender was
added to the models if performance differed between the sexes
or if linear trends for one or more of the factors was modified
in the models because many of the non-AG participants were
found to have spent at least 2 years working in agriculture.
Participants with incomplete data on a neurobehavioral
performance test were excluded from the analysis of that test.
A total of 175 individuals completed the neurobehavioral
test battery (Table 2). Seventy-two percent of the non-AG
adults and 37% of the non-AG adolescents report working in
agriculture in the past. In fact, five non-AG participants had at
least 8 years of agricultural experience with two reporting 10
years and one reporting 14 years.
Thirty-eight participants report that they have mixed and/or
applied pesticides in the past, and 17 participants have mixedor
applied pesticides in the past month. The majority of
participants handling pesticides are male and work in
agriculture, although non-AG participants and females also
report handling pesticides. The frequency of using protective
clothing for the 16 male participants who report handling
pesticides in the past month are presented in Table 3.
The majority of participants completed all of the neurobe-
havioral tests (Table 4), however, adult female participants
working in agriculture had lower completion rates (75% of the
neurobehavioral tests) compared to other groups (t173= 4.48,
p < 0.001) that had an average of 88% completion rate. A large
percentage of all participants were unable to complete the
Reversal Learning test (approximately 68%). This was the last
test presented in the lengthy battery and often participants did
not have enough time to complete the test. The data from this
test were excluded from the subsequent analyses.
The impact of age, years of education, gender and years
working in agriculture was examined on each neurobehavioral
measure. Table 5 presents the estimated slope (b-coefficient)
showing the average change in each neurobehavioral measure
per 5-year increase in the indicated predictor (age, years of
education, years working in agriculture).
3.1. Age and neurobehavioral performance
Age was a major predictor of performance on Finger
Serial Digit Learning tests. As the age of the participants
increased the performance on the neurobehavioral test
decreased (Table 5). For example, performance on Finger
Neurobehavioral tests, outcome measures and functions being tested in the
Neurobehavioral test (outcome measure)Function
Finger Tapping (number of taps)Response speed,
Simple Reaction Time (latency)
Digit Span (correct score)
Progressive Ratio (number of taps)
Selective Attention (number of trials, latency)
Serial Digit Learning (score)
Continuous Performance (percent hits, percent
false alarms, percent omissions, d-prime)
Match-to-Sample (score, latency)
Reversal Learning (trials to criterion)
D.S. Rohlman et al./NeuroToxicology 28 (2007) 374–380376
Tapping (preferred hand) decreases an average of 2.4 taps for
each 5-year increase in age. In addition, an interaction between
age and gender was found for the Selective Attention Test
(number of trials, latency). The older the female participants,
the more performance on the Selective Attention measures
decreased. The only measure that had improved performance
for the adults was the d-prime measure of the Continuous
Performance test (a measure of attentiveness, how well a
participant distinguishes between targets and non-targets). In
general, older subjects (35) tended to have slightly higher
scores than did younger subjects with similar years spent
working in agriculture. For those older subjects, scores
appeared to increase with increasing years spent working in
agriculture; for younger subjects, average scores tended to
3.2. Education and neurobehavioral performance
Years of education in the participant’s country of origin was
found to have a significant main effect on Digit Span (forward
and reverse), Finger Tapping (alternating trials), Symbol-Digit,
Reaction Time, Selective Attention (latency), Serial Digit
Learning, Match-to-Sample (score), and Continuous Perfor-
mance (Table 5). In each case as years of education increased
performance on these measures improved.
3.3. Gender and neurobehavioral performance
A significant main effect of gender was found on the Finger
Tapping (preferred, non-preferred, and alternating trials) and
Progressive Ratio Tests with females performing worse than
males on these two tests (Table 5).
3.4. Years of agricultural work and neurobehavioral
A significant main effect of years working in agriculturewas
found for Match-to-Sample (score), as years spent working in
agriculture increased performance decreased. An interaction
between age and years working in agriculture was found for
have slightly better scores than younger participants with
similar years spent working in agriculture.
Gender was also found to interact significantly with years
working in agriculture on the Symbol-Digit, Reaction Time,
and (for male participants) Selective Attention tests. For
females, as years working in agriculture increased, perfor-
mance on the Symbol-Digit and Reaction Time measures
Demographic characteristics of participants completing the neurobehavioral test battery
Adult AG, n = 69 Adolescent AG, n = 50 Adult non-AG, n = 29Adolescent non-AG, n = 27
Age (mean and S.D.)28.2 (7.6) 15.7 (1.6) 30.7 (8.4)14.7 (1.8)
Percent female (%)33.3 30.051.7 51.9
Education (years) (mean and S.D.) in
Country of origin
Any education in US (%)4 3014 85
Years working agriculture (mean and S.D.)
Ever worked in agriculture (%)
Mix/apply pesticides (number and %)
Years in agriculture (mean)
Mix/apply past month (number)
Mix/apply pesticides (number and %)
Years in agriculture (mean)
Mix/apply past month (number)
Frequency of use of protective clothing or equipment for male participants who
reported mixing or applying pesticides in the past month (n = 16)
Goggles or glasses
Other protective clothinga
aHandkerchief or support belt.
Percentage of tests completed by participants
Adult AGAdult non-AG Teen AGTeen non-AG
*Adult female participants working in agriculture had significantly lower
completion rates than the other groups.
D.S. Rohlman et al./NeuroToxicology 28 (2007) 374–380377
decreased; this effect was not significant for males. For males
there was no effect on Symbol-Digit or Reaction Time.
However, there was a compound effect of age and years
working in agriculture for the males (linear ? linear interac-
tion). As both age and years of working in agriculture increased
in males, performance on the Selective Attention measures
decreased. For females, as age increased, performance on the
Selective Attention measures decreased.
3.5. Pesticide handling and neurobehavioral performance
Neurobehavioral performance was examined in men
(n = 108) to determine whether differences existed among
three groups: those without any experience mixing/applying
pesticides (68%; n = 74), those with any prior experience of
mixing/applying pesticides (31%; n = 34) and a subset of the
previous group of men who had mixed/applied pesticides in the
month prior to testing (15%; n = 16). Multiple linear regression
was used to control for differences due to age, years of
education, and years spent working in agriculture. The
expectation was for mixing/applying pesticides to lower
neurobehavioral performance; consequently, one-sided p-
values were used in comparing groups with some prior
experience mixing/applying pesticides against the baseline
group of non-mixer/applicators. Reported effects and/or
changes reflect those for a 21-year-old man with 4 years of
agricultural work experience and 5 years of education in his
country of origin.
Any experience of mixing/applying pesticides was found to
significantly decrease performance on four neurobehavioral
measures. Scores on Digit Span forward and Digit Span reverse
were significantly lower for men who had handled pesticides
Estimated slope (b-coefficient) showing the average increase or decrease in each neurobehavioral measure per 5-year increase in the indicated predictor (years
working in agriculture, years of education, age)
Neurobehavioral measureYears in agricultureYears of education AgeNotes
Latency M: ?10 (0.57)
F: 480 (<0.01)
?300 (<0.01) 155 (0.99)
?0.61 (0.03)0.75 (0.05)
Latency M: ?12 (0.94)
F: 32 (<0.01)
F: ?12 (?0.96)
M: ?5.9 (0.12)
F: 19 (0.99)
AG ? aged
Serial Digit Learn
0.6 (<0.01)AG ? agee
Number of tapsGenderf
Negativevalues for latency measures (Symbol-Digit, Reaction Time, Selective Attention) indicate improved performance. Measures that showed an interaction with
gender are described separately for males (M) and females (F). One sided p-values are given in parentheses.
aSignificant overall effect due to sex (p < 0.01); females averaged 17.4 fewer taps than males.
bSignificant overall effect due to sex (p < 0.01); females averaged 11.7 fewer taps than males.
cSignificant overall effect due to sex (p < 0.01); females averaged 13.2 fewer taps than males.
dMales showed an interaction between age and years in agriculture (p = 0.01); performance worsened for males as both age and years in agriculture increase
eSignificant interactionbetween ageand years in agriculture (p = 0.04);for older participants(?35), scoresincreased as bothage and yearsin agriculture increase
fSignificant overall effect due to sex (p < 0.01); females averaged 87 points lower than males.
D.S. Rohlman et al./NeuroToxicology 28 (2007) 374–380378
(0.51 points lower for forward, p = 0.02 and 0.52 points lower
for reverse, p = 0.02). Match-to-Sample scores were also lower
(2.04 points) for men who reported handling pesticides in the
past compared to men who had never reported handling
pesticides (p = 0.02). The percentage of hits on the Continuous
Performance test also showed a decrease for men who handled
pesticides (6.4 percentage points, p = 0.047). Although not
significant, performance was also decreased on Serial Digit
Learning (2.02 points lower among men who had handled
pesticides; p = 0.09) and Symbol-Digit (average latency
135 ms greater, p = 0.21). The Progressive Ratio test showed
improved performance for men who had handled pesticides in
the past (41.7 points higher).
When the subset of participants who had recent experience
mixing/applying pesticides was compared to the participants
who had no experience handling pesticides, three neurobeha-
vioral measures showed decreased performance. Men who
reported mixing/applying pesticides in the past month had an
average Match-to-Sample score 2.68 points lower than
(p = 0.015). The percentage of hits and d-prime score for
the Continuous Performance test also showed decreased
performance, 15.8 percentage points on percent hits and 0.79
points lower on d-prime score, for men mixing/applying
pesticides in the past month compared to men with no pesticide
handling (p = 0.001 and p = 0.012, respectively). The Pro-
gressive Ratio test showed that men who had recent experience
mixing/applying pesticides had improved performance (25.8
more taps) compared to men with no experience handling
pesticides (one-sided p-value = 0.85).
The present study presents an analysis of results on
neurobehavioral tests among a population of adolescent and
adult farmworkers and comparison groups. Age, school
performance on the neurobehavioral tests. Pesticide handling
was also associated with performance on the neurobehavioral
Age had an impact on the Finger Tapping, Symbol-Digit,
Selective Attention and the Continuous Performance (d-prime)
tests. With the exception of Continuous Performance, older
participants performed worse than younger participants. Years
of education had a significant impact on performance on eight
out of nine neurobehavioral tests. As years of education
increased, performance on the neurobehavioral tests improved.
Gender also had an impact on performance. On the motor
tests, Finger Tapping and ProgressiveRatio, females performed
worse than males. This is consistent with Anger et al. (1997)
who also found an effect of gender on a tapping measure in the
These findings suggest that years working in agriculture also
impacted performance. More years working in agriculture was
associated with worse performance on the Match-to-Sample,
Symbol-Digit, Reaction Time, and Selective Attention tests.
There also appears to be an interaction between years working
gender effects were reported in an earlier study conducted in
1999 (Rothlein et al., 2006). While gender differences have
been noted on specific neurobehavioral tests, these results and
earlier findings suggest that there may be a differential impact
from agricultural work as well. Other studies have also found
lower performance on neurobehavioral tests associated with
increased years working in agriculture (Kamel et al., 2003;
Rolda ´n-Tapia et al., 2005). Participants chronically exposed to
pesticides for more than 10 years had lower performance on
measures of perception and visuospatial processing (Rolda ´n-
Tapia et al., 2005). This study also showed no correlation
between plasma cholinesterase, a measure of recent exposure,
and cognitive deficits. Kamel et al. (2003) also found that the
greatest decrease in cognitive and psychomotor functions was
observed after 10 or more years of work.
Handling pesticides also impacted neurobehavioral perfor-
mance. Thirty-four participants report mixing and applying
pesticides. More males than females (34 versus 4) and more
adults than adolescents (30 versus 8) reported handling
pesticides. The years working in agriculture were very similar
for the adult male participants who never handled pesticides
(10.6 years and 2.1 years for the AG and non-AG groups)
compared to the adult male participants who report mixing/
AG groups). However, the male adolescent participants who
(2.8 years and 1.5 years for the AG and non-AG groups)
compared to the male adolescents who report mixing/applying
pesticides (8.0 years and 5.5 years for the AG and non-AG
groups). Personal protective equipment use was reported to be
infrequent or not at all in the male participants who handled
pesticides in the past month. Performance deficits associated
with pesticide handling were found on the Digit Span, Match-
to-Sample, and Continuous Performance Tests.
demographic variables such as age, education, and gender have
been known to impact performance on neurobehavioral tests
(Anger et al., 1997). Several neurobehavioral measures were
significantly affected by the gender of the participant. Previous
studies of neurobehavioral performance in farmworkers have
generally assumed that observed deficits are a result of pesticide
exposure (Kamel et al., 2003) and significant gender effects in
humans have not been reported. Rothlein et al. (2006) reported
gender differences on FingerTapping, Serial Digit Learning and
an overall summary index of neurobehavioral performance in
Oregon farmworkers. Furthermore, several findings examining
effects of gender (Dam et al., 2000; Levin et al., 2001, 2002).
Further research is warranted to examine the impact of gender.
These findings do not provide evidence that adolescents
these tests than their adult counterparts. However, the results are
limited in that no exposure variables are available other than
years of working in agriculture and self-reported pesticides use.
The results of four tests (Match-to-Sample, Selective Attention,
Symbol-Digit, and Reaction Time) add to the increasing
D.S. Rohlman et al./NeuroToxicology 28 (2007) 374–380379
evidence that neurological impairment may be associated with Download full-text
increased years working inagriculture. Furthermore, the deficits
found in the participants who reported handling pesticides
compared to those with no experience indicate the potential
impact of pesticide exposure. Time and exposure levels need to
be examined to determine the dose–effect relationship. Long-
itudinal studies are needed to document if earlier onset of
agricultural work results in increased deficits as a cohort ages.
This publicationwas supported by funding from the National
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