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Health Effects Associated With Sulfuryl

Fluoride and Methyl Bromide Exposure


Among Structural Fumigation Workers

Geoffrey M. Calvert, MD, MPH, Charles A. Mueller, MS, John M. Fajen, MS,
David W. Chrislip, John Russo, PhD, Thomas Briggle, PhD, Lora E. Fleming, MD, PhD,
Anthony J. Suruda, MD, MPH, and Kyle Steenland, PhD

Methyl bromide and sulfuryl fluoride 123 structural fumigation workers in south
are commonly used fumigants. Methyl bro- Florida. Data were collected and analyzed to
mide is widely used in Florida and California determine whether chronic, generally low-
for agricultural pest control and, until level exposure to these fumigants was associ-
recently, was also widely used in structural ated with nervous system (central and periph-
pest control. Because of concerns about eral), renal, or pulmonary effects. This is the
>- stratospheric ozone depletion, the US Envi- largest known health study of workers
ronmental Protection Agency has proposed a exposed to these fumigants.
phaseout of methyl bromide production and
....; use by the year 2001.1 In the early 1990s,
sulfuryl fluoride replaced methyl bromide as Methods
the fumigant most commonly used in struc-
tural termite control. This study compared health outcomes
Methyl bromide is extremely toxic after among workers employed at the time of the
acute, high-intensity exposure. Neurological study as shooters (individuals who introduced
manifestations from acute methyl bromide the fiumigant into a structure) and tent crew
poisoning include ataxia, behavioral changes, workers (individuals who raised and disman-
.: seizures, and coma.2 However, little is known tled the tarps used to cover fumigated struc-
about the effects of chronic, low-level expo- tures to prevent fumigant leakage) in the
sure to methyl bromide. Case reports of structural fumigation industry with health out-
I;: workers chronically exposed to methyl bro- comes in an unexposed referent (comparison)
mide have described electroencephalogram group. Fumigant exposure in this industry is
abnormalities3 and peripheral neuropathy,3'4 intermittent (generally less than 2 hours per
and a cross-sectional study found that work- day) and is considered to occur potentially
MN'.$sz.$ ers with low-level methyl bromide exposures
had statistically significant deficits on the
.i Wechsler Memory Scale and on 2-point dis-
Geoffrey M. Calvert, Charles A. Mueller, John M.
cnimination at the index fnger.5 Fajen, and Kyle Steenland are with the Division of
ig Less is known about the toxicity of sul- Surveillance, Hazard Evaluations and Field Studies,
Fi. furyl fluoride. Fatalities have been reported National Institute for Occupational Safety and
from acute poisoning.6'7 In addition, rats Health, Centers for Disease Control and Prevention,
exposed to high levels of sulfuryl fluoride Cincinnati, Ohio. David W. Chrislip and John Russo
Xa .: experienced neurological, pulmonary, and are with the Division of Behavioral and Biomedical
renal toxicity.8 A study of workers with low- Sciences, National Institute for Occupational Safety
and Health, Cincinnati, Ohio. Thomas Briggle and
level sulfuryl fluoride exposures found non- Lora E. Fleming are with the Department of Epi-
sigiflcantly reduced performance on all neu- emiology and Public Health, University of Miami
robehavioral tests compared with the referent School of Medicine, Miami, Fla. Anthony J. Suruda
is with the Rocky Mountain Center for Occupational
group. and Environmental Health, University of Utah, Salt
To address the need for additional infor-
|!$.. mation on the toxicity of methyl bromide and Lake City.
Correspondence and requests for reprints
sulfuryl fluoride, the National Institute for should be sent to Geoffrey M. Calvert, MD, MPH,
Occupational Safety and Health (NIOSH) NIOSH, 4676 Columbia Parkway, R-21, Cincin-
and the University of Miami conducted a nati, OH 45226 (e-mail: jac6(cdc.gov).
cross-sectional study in 1992 and 1993 of This paper was accepted June 2, 1998.

December 1998, Vol. 88, No. 12


Health Effects Among Structural Fumigation Workers

when the fumigant is introduced into the (median and ulnar) and 2 nerves of the non- The Santa Ana Dexterity Test, a non-
building and when the tarps are dismantled. dominant lower limb (peroneal and sural). In coinputerized test of psychomotor function,
The workers were employed at the time addition, f latencies were measured on the required turning rows of successive pegs 180
of the study at one of 40 fumigation compa- peroneal motor nerve. All tests were per- degrees.'4 The total number of pegs turned in
nies located in the Miami and Tampa/St. formed with surface electrodes. The surface two 30-second trials per hand was recorded.
Petersburg, Fla, metropolitan areas. These temperature was maintained at 32°C to 34°C Postural sway testing, a computerized
companies were chosen because they were for the upper limb and at 30°C to 33.5°C for version of the Romberg test, was conducted
performing many fumigation jobs and the lower limb. If necessary, limb tempera- with a fixed strain-gauge-type force platform
because they used predominantly one type of ture was raised and maintained with an elec- (Advanced Mechanical Technologies, New-
fumigant. To qualify for participation, work- tric heating pad. ton, Mass).'5 Four 30-second tests were com-
ers from these companies had to report in a Vibration testing consisted of measure- pleted for each participant (standing on a hard
screening interview that they had been ment of vibrotactile thresholds in the non- surface with his eyes open then repeated with
employed in the fumigation industry for at dominant index finger and great toe with the eyes closed, and standing on a soft foam pad
least the preceding 6 months; that they were Vibratron II device (Physitemp Instruments, with his eyes open then repeated with eyes
currently engaged in fumigation activities at Clifton, NJ) and a "trimmed 2-5 method of closed). Ratios between the various measure-
least 80% of the time; and that among the limits" protocol.""2 Five trials (3 descending ments were also calculated, as previously
fumigation jobs they had ever participated and 2 ascending) were performed on each described.'6
in, the fumigant involved was either (1) sul- limb. The first trial and the trials with the Contrast sensitivity, a test of visual
fuiryl fluoride on 80% or more of the fumiga- highest and lowest measurements were dis- function, was assessed with the Pelli-Robson
tion jobs or (2) methyl bromide on 50% or carded. The 2 remaining measurements were chart, which consists of 16 rows of 3 let-
more of the fumigation jobs (because use of averaged and recorded. ters.'7 The rows decrease in contrast from
methyl bromide was declining rapidly at the Seven supervised, computer-adminis- top to bottom. Each eye was tested sepa-
time of our study, a lower proportion was tered neurobehavioral tests from the Neuro- rately, and a separate chart (with a different
used). All worker participants were male. behavioral Evaluation System (NES), ver- arrangement of letters) was used for the left
The referent group was recruited by the sion 4.33, were conducted.'3 These tests and right eyes. Contrast sensitivity was
fumigation workers. Each worker was asked required a reading level equivalent to an ele- scored as the row with the faintest contrast in
to identify a male friend or neighbor who was mentary school education. The 7 tests are which 2 of the 3 letters were correctly identi-
a similar age (+ 5 years), who had never described below: fied. Color vision was assessed with the
worked as a pesticide applicator or in the 1. Hand-eye Coordination. Measured Farnsworth D-15 panel test.'8 This test con-
fiumigation industry, and who had never been the degree of error when using a joystick to sists of 15 movable caps, each of a different
poisoned by pesticides. All participants were trace wave patterns projected on the com- color. The participant was asked to line up
paid $150 as compensation for their time and puter screen. the caps in sequential color order. Each eye
effort. NIOSH Human Subjects Review 2. Simple Reaction Time. Measured the was tested separately. The test was scored as
Board and the University of Miami Institu- response time for pressing a key when pro- abnormal if the arrangement of caps was
tional Review Board approved the study pro- vided a randomly timed visual stimulus. consistent with 1 of 3 types of color vision
tocol. Informed consent was obtained from 3. Continuous Performance Test. defect. A retroilluminated Snellen letter chart
all participants. Required the participant to press a key when was used to measure visual acuity.
Information on each study participant a certain letter appeared amid a temporal Olfactory function was tested with the
was collected through a comprehensive stan- sequence of letters. Response time and non- University of Pennsylvania Smell Identifi-
dardized questionnaire and a set of medical responses were analyzed. cation Test (UPSIT) (Sensonics, Inc, Had-
tests. To reduce observer bias, all test admin- 4. Symbol Digit Test. Required rapid donfield, NJ). 9 This standardized, self-
istrators were blinded to exposure status. pairing of digits to symbols according to an administered smell test involves 40
Study instructions, questionnaires, and tests exhibited matched pairing. Immediately fol- microencapsulated odorants. The partici-
were administered in English or Spanish lowing testing, the number of pairings that pant was asked to identify the odor of each
according to the participant's preference were memorized was also recorded. odorant from a list of 4 choices. The 4
(with the exception of the vocabulary test, 5. Pattern Memory. Required selecting choices were read to illiterate participants
which was administered only in English). a previously seen pattern out of 3 similar pat- by one of the study staff. The number of
Lifetime occupational and medical history terns. The proportion of correctly identified correctly identified odors was recorded.
information was obtained through an inter- patterns and the mean recall time were Because 28 participants (14 workers and 14
viewer-administered questionnaire. Detailed recorded. referents) did not provide a response to all
information on fumigation industry employ- 6. Serial Digit Learning. Required 40 odors, all tests were also scored as the
ment was collected for both the year preced- memorizing a series of 8 digits. The number proportion of odors responded to that were
ing the worker's examination and the of trials required to memorize the 8 digits correctly identified.
worker's entire duration of funigation indus- was recorded.
try employment.9 7. Mood Scales. Evaluated 5 different Other Examinations
self-reported mood categories (anger, con-
Tests of Neurological Function fusion, depression, fatigue, and tension/ Spot urine samples were collected and
anxiety). analyzed for total protein, albumin, and
Nerve conduction tests to detect periph- In addition, the NES vocabulary test adenosine deaminase binding protein. Partic-
eral neuropathy were administered by means was administered to participants taking the ipants were evaluated for chronic bronchitis
of documented techniques.'0 Nerve conduc- English version of the NES. For each of 25 with questions recommended by the Ameri-
tion velocities and amplitude were measured words, the participant had to select the cor- can Thoracic Society.20 Finally, a physician
on 2 nerves of the nondominant upper limb rect synonym from a list of 4 words. completed a physical examination of the

December 1998, Vol. 88, No. 12 American Journal of Public Health 1775
Calvert et al.

neurological system to detect gross abnor- exposure and low methyl bromide years of SAS procedures (SAS Institute Inc,
malities of the motor, sensory, and cerebellar exposure. The lifetime duration of sulfuryl Cary, NC) were used for all analyses. A P
systems. The findings from this examination fluoride exposure was calculated in a similar value of .05 or less was considered statisti-
were used to screen for neurological prob- way (sulfuryl fluoride years). cally significant.
lems unrelated to fumigant exposure (e.g., To assess the effect of exposures during
trauma or stroke). the year preceding the worker's examination,
workers were defined as having either high Results
Data Analysis sulfuryl fluoride exposure (if the worker
used sulfuiryl fluoride on more than 50% of Of the 196 workers employed at the 40
The Student t test was used in the analy- jobs during the previous year) or high methyl structural fumigation companies chosen for
sis of continuous demographic characteristics. bromide exposure (if the worker used methyl study participation, 49 (25%) were deter-
Chi-square statistics were used to compare bromide on 50% or more of jobs during the mined by the screening interview to be ineli-
categorical demographic characteristics and previous year). These exposure groups were gible for the study. A total of 123 of 147
outcomes. (The Fisher exact test was used compared with the referent group. Four (84%) of the eligible structural fumigation
when any of the expected table frequencies workers were excluded from the preceding workers and 120 referents participated.
were less than 5.) year analyses because they had worked less Descriptive information on the study partici-
Multiple linear regression analyses than 6 months in structural fumigation dur- pants is provided in Table 1. The fumigation
were performed. Confounders were identi- ing that year. workers and referents were generally similar,
fied a priori by a review of the literature. For many of the analyses, some partici- but the referents had significantly longer
Regression models for the nerve conduction pants were excluded a priori. Nine partici- schooling. Among fumigation workers, the
tests included age, race, body mass index, pants (5 workers, 4 referents) were excluded median duration of employment in structural
and limb surface temperature. Regression from analysis of the computerized neurobe- fiunigation was 4.0 years. The median life-
models for vibration testing included age, havioral data, most (n = 7) because of insuf- time duration of methyl bromide and sulfuiryl
race, and height. Models for the computer- ficient reading ability. A few participants fluoride exposure was 1.20 years and 2.85
ized neurobehavioral tests included age, were excluded from specific tests for reasons years, respectively.
years of education, and the language in such as malfunction of equipment or report On average, fumigation workers per-
which the test was taken. Regression models of a physician-diagnosed health problem that formed worse on all tests of median nerve
for the Santa Ana Dexterity Test included was unrelated to fumigant exposure but that function than did the referents, but only 1 of
age and race. Models for the postural sway could affect test performance. these tests was statistically significant
data included age, race, number of alcoholic
drinks consumed per week, height, and
weight. Models for contrast sensitivity TABLE 1-Characteristics of the Study Participants Fumigation Workers:
included age, visual acuity, and years of edu- South Florida, 1992-1993
cation. Regression models for UPSIT Fumigation workers Referents
included smoking status (current smoker, (n= 123) (n = 120)
former smoker, never smoker), years of edu-
cation, and race. Finally, models for tests of Mean age, y (range) 33 (19-68) 31 (18-58)
renal function included age, years of educa- Race/ethnicity, no. (%)
White 52 (42) 54 (45)
tion, and race. Findings were similar when Black 44 (36) 42 (35)
premorbid intellectual ability was controlled Hispanic 27 (22) 24 (20)
by using the NES vocabulary test score Mean years of education* (range) 11.5 (0-19) 12.3 (0-17)
instead of years of education. However, Spanish was preferred language, %a 8.9 5.0
Mean body mass index (range)b 26 (18-41) 26 (18-49)
because the NES vocabulary test score was Mean height, in (range) 70 (57-76) 70 (57-76)
not available for 17 participants, results are Smoking status, no. (%)
provided only from those models containing Current 56 (46) 47 (39)
years ofeducation. Former 13 (11) 10 (8)
Never 54 (44) 63 (53)
Several measures of exposure were Alcohol status, no. (%)
used in the analyses. Employment as a struc- Current 92 (75) 84 (70)
tural fumigator was used as a dichotomous Former 18 (15) 22 (18)
exposure variable (defined as being a fumi- Never 13 (10) 14 (12)
gation worker or not). Additionally, separate Mean no. of alcoholic drinks consumed
per wk (range) 13 (0-168) 10 (0-84)
measures of exposure for each fumigant Median years of employment in structural
were created and are described in detail else- fumigation (range) 4.00 (0.5-32) 0
where.9 Briefly, the lifetime duration of Median methyl bromide years (range)c 1.20 (0-22.1) 0
methyl bromide exposure for each worker Median sulfuryl fluoride years (range)d 2.85 (0.11-20.5) 0
was calculated as the product of his self- aLanguage chosen for the computerized neurobehavioral test; 9 participants did not take
reported years of fumigation industry this test.
employment and his self-reported lifetime bWeight in kilograms divided by height in meters squared.
proportion of fumigation jobs that used CThe product of self-reported years of structural fumigation employment and lifetime
methyl bromide. Methyl bromide-exposed proportion of fumigation jobs that used methyl bromide.
dThe product of self-reported years of structural fumigation employment and lifetime
workers were stratified into 2 groups based proportion of fumigation jobs that used sulfuryl fluoride.
on the median years of methyl bromide *Significant difference at the P = .05 level.
exposure: high methyl bromide years of

1776 American Journal of Public Health December 1998, Vol. 88, No. 12
Health Effects Among Structural Fumigation Workers

TABLE 2-Multiple Linear Regression Results Comparing Nerve Conduction Velocity (NCV), Amplitudes, and Vibration
Threshold Among Structural Fumigation Workers vs Unexposed Referents: South Florida, 1992-1993
Worse Performance
Fumigation Worker Referent P Value for Direction of With Increasing
Adjusted Adjusted Adjusted Worker Duration of
Test n Meana n Meana Analysis Performanceb Fumigant Exposurec
Upper limbd
NCV (distal): median sensory, m/s 121 52.9 120 54.3 .16
NCV (forearm): median sensory, m/s 121 60.4 120 61.1 .41
NCV (forearm): median motor, m/s 121 54.6 120 55.9 .02 _ SF
NCV (distal): ulnar sensory, m/s 122 53.2 120 51.8 .06 +
Amplitude: median sensory, pV 121 27.0 120 29.2 .12 - MB, SF
Amplitude: median motor, mV 120 10.6 119 11.1 .30 - SF
Amplitude: ulnar sensory, pV 122 23.8 120 23.9 .97
Vibration threshold: finger, pm peak to peak 121 1.07 120 1.10 .81 +
Lower limbe
NCV: peroneal motor, m/s 120 46.3 115 46.6 .51
NCV: sural sensory, m/s 119 46.0 113 44.9 .07 +
Amplitude: peroneal motor, mV 118 6.81 115 6.78 .95 +
Amplitude: sural sensory, pV 118 17.3 113 15.6 .06 +
f latency: peroneal motor, ms 119 49.9 115 50.1 .64 +
Vibration threshold: toe, pm peak to peak 120 3.90 114 4.28 .55 +
aModels for nerve conduction tests controlled for age, race, body mass index, and temperature of the limb. Models for vibration threshold
controlled for age, race, and height.
+= Performance of workers was better vs referents based on adjusted means. - = Performance of workers was worse vs referents based on
adjusted means.
CSF = based on adjusted analyses, as sulfuryl fluoride exposure increased (referent, low sulfuryl fluoride years of exposure, high sulfuryl
fluoride years of exposure), monotonically decreasing performance was observed.
MB = based on adjusted analyses, as methyl bromide exposure increased (referent, low methyl bromide years of exposure, high methyl
bromide years of exposure), monotonically decreasing performance was observed.
dThe "distal" measurement is the NCV from the wrist to the interdigital cleft, and the forearm measurement of the median nerve is the NCV
from the elbow to the wrist.
eNCV of the peroneal nerve was measured from the knees to the ankle, and the sural nerve velocity was measured from the mid-calf to the
ankle. The fastest of at least 10 f latency responses was recorded.

(slower nerve conduction velocity of the (Table 4). This finding may more likely be Discussion
median motor nerve in the forearm, P = .02) associated with the ergonomic stresses (e.g.,
(Tables 2 and 3). In addition, 8 workers and repetition, force, and awkward joint position) This study suggests that employment as
4 referents had nerve conduction velocity among tent crew workers over the year pre- a structural fumigation worker is associated
findings consistent with carpal tunnel syn- ceding examination than with sulfiuyl fluo- with some adverse effects on the central and
drome (the ratio of conduction velocity of ride exposure. This is because preferred-hand peripheral nervous systems. With respect to
the distal ulnar nerve to conduction velocity Santa Ana performance was lower among the peripheral nervous system, performance
of the distal median nerve exceeded 1.25, these "currently" employed tent crew work- was reduced on the Santa Ana Dexterity Test
and conduction velocity of the distal median ers than among fumigation workers not cur- and on all tests of median nerve function,
nerve was less than 50 m/sec). All 8 of the rently employed as tent crew workers and the prevalence of carpal tunnel syn-
fumigation workers with carpal tunnel syn- (P= .06), whereas no significant difference drome was higher among workers compared
drome were tent crew workers at the time of was found among these 2 groups of fumiga- with referents. The median nerve effects
examination, and all 8 denied ever being a tion workers in the proportion of jobs that experienced by workers are most likely
shooter. used sulfuryl fluoride in the preceding year caused by workplace ergonomic factors such
Pattem Memory was the only computer- (P= .31). as repetitive, forceful squeezing of heavy-
administered neurobehavioral test on which Deficits on UPSIT performance were duty spring clamps used to fasten tarps that
workers had significantly worse performance particularly evident among workers with cover a fumigated structure and other repeti-
than did referents. Although this finding was high sulfuiryl fluoride exposure over the pre- tive tasks involved in raising and disman-
especially evident among workers with high ceding year (Table 4) (adjusted mean UPSIT tling tarps. The role of these ergonomic fac-
sulfuryl fluoride exposure during the year score: workers with high sulfuryl fluoride tors is supported by the decrements observed
preceding examination (Table 4), a trend of exposure = 33.1, referents = 34.4, P = .03), in preferred-hand Santa Ana Dexterity Test
worse performance with increasing lifetime suggesting that sulfuryl fluoride exposure performance among tent crew workers.
duration of sulfuryl fluoride exposure was may be associated with adverse effects on Those in occupations that place them at risk
also observed (Table 5). Fumigation workers olfactory function. No significant differences for repetitive trauma disorders have reduced
also had reduced performance on the Santa were found between fumigation workers and performance on Santa Ana testing.2' In the
Ana Dexterity Test when the preferred hand referents for chronic bronchitis, for any of absence of significant findings involving any
was tested (Table 5), and more specifically the urinary protein concentrations, or for per- of the other upper- or lower-extremity
among workers with high sulfuryl fluoride formance on the color vision test or the pos- peripheral nerves, it is unlikely that fumigant
exposure in the year preceding examination tural sway tests (data not shown). exposure is responsible for the median nerve

December 1998, Vol. 88, No. 12 American Journal of Public Health 1777
Calvert et al.

TABLE 3-Multiple Linear Regression Results Comparing Nerve Conduction Velocity (NCV), Amplitudes, and Vibration
Threshold Among Structural Fumigation Workers With High Methyl Bromide Exposure or High Sulfuryl Fluoride
Exposure During the Year Preceding Examination vs Unexposed Referentsa: South Florida, 1992-1993
Workers With High Methyl Workers With High Sulfuryl
Bromide Exposure Over the Year Fluoride Exposure Over the Year
Preceding Examination (n = 28) Preceding Examination (n = 91)
Direction of Workers With High Direction of Workers With High
Methyl Bromide Exposure Sulfuryl Fluoride Exposure
Test Compared With the Referent Groupb P Compared With the Referent Groupb p
Upper limb
NCV (distal): median sensory - .78 .10
NCV (forearm): median sensory - .20 .75
NCV (forearm): median motor - .40 .02
NCV (distal): ulnar sensory + .35 + .08
Amplitude: median sensory - .06 .34
Amplitude: median motor + .59 .09
Amplitude: ulnar sensory - .21 + .68
Vibration threshold: finger + .84 + .85
Lower limb
NCV: peroneal motor - .40 .77
NCV: sural sensory + .07 + .21
Amplitude: peroneal motor + .94 + .88
Amplitude: sural sensory + .03 + .20
f latency: peroneal motor + .42 + .86
Vibration threshold: toe + .56 + .65
aWorkers with high methyl bromide exposure and high sulfuryl fluoride exposure are defined as workers who used each substance on 50% or
more of jobs. Models for nerve conduction tests controlled for age, race, body mass index, and temperature of the limb. Models for vibration
threshold controlled for age, race, and height.
+ = Performance of fumigation workers was better vs referents based on adjusted means. - = Performance of fumigation workers was worse
vs referents based on adjusted means.

findings in our study. Based on the pattern of reduced performance on all cognitive tests sent interference of the odor/receptor interac-
neurotoxicity produced by high methyl bro- compared with the referent group. Methyl tion or a cognitive problem with odor iden-
mide exposure, initial involvement of the bromide exposure was associated with signif- tity. Although small amounts of chloropicrin,
nerves in the lower extremity is expected.2223 icantly worse performance on the Logical an irritant, are used as a warning agent during
Although one median nerve outcome (nerve Memory test of the Wechsler Memory Scale sulfiryl fluoride and methyl bromide fumiga-
conduction velocity of the median motor (this test measures ability to recall details of a tions, chloropicrin is not likely to be responsi-
nerve in the forearm) was associated with story read aloud). These workers had higher ble for our olfactory findings, because differ-
exposure to sulfuiryl fluoride, this may be an median years of employment in fumigation ences in effect from the 2 fumigants should
isolated chance finding caused by the large occupations and may have used methyl bro- not have been observed.
number of comparisons that were performed. mide on a higher proportion of fumigation Note that the intensity of fumigant ex-
We found limited data to suggest fumi- jobs compared with the workers we studied. posure among structural fumigation workers is
gant exposure effects on neurobehavioral However, this study had several limitations low, based on personal airborne sampling con-
function. However, we did find that workers (e.g., significant schooling differences ducted by NIOSH in 1991. Among structunal
with high sulfuryl fluoride exposure in the existed between methyl bromide-exposed fumigation workers, all personal airborne sam-
previous year had significantly reduced per- workers and referents, and the Wechsler pling results for sulfiuyl fluoride and most for
formance on the Pattern Memory Test (Table Memory Scale was administered only in methyl bromide were below the Occupational
4). Because the Pattern Memory Test is a test English even though Mexican Americans Safety and Health Administration pennissible
of cognitive and visual memory,24 these find- constituted a higher proportion of methyl exposure limits in effect at the time of sam-
ings suggest that sulfuryl fluoride exposure bromide-exposed workers compared with pling (20 mg/m3 time-weighted 8-hour aver-
may be associated with deficits in this area. referents [38% vs 7%, respectively]).5 age). Furthermore, more than two thirds of the
Although none of the other memory tests in Our study found that sulfuryl fluoride measurements were below the limit of detec-
this study (e.g., Symbol Digit Recall score exposure may be associated with effects on tion (sulfuryl fluoride = 0.007 mg/sample;
and Serial Digit Learning score) were associ- olfactory function, an outcome not previously methyl bromide = 0.01 mg/sample). However,
ated with sulfiuyl fluoride exposure, this may assessed in human studies of sulfuryl fluoride because the NIOSH-recommended analytic
not be unexpected. Sulfiuyl fluoride may be exposure. One animal study found that high method for measuring methyl bromide may
altering information-processing abilities that sulfuryl fluoride exposure is associated with underestimate its concentration,26 we predict
are required only in the Pattern Memory Test. inflammation of nasal tissues25; however, that some fumigation workers may have had
Also, the pattern memory findings may have effects on olfactory function or olfactory periodic short-term exposures to methyl bro-
arisen by chance. mucosa among animals have not been mide exceeding 80 mg/m3 (the current pennis-
One other study examined neurobehav- reported. Further study is needed to deter- sible exposure limit27). No important work
ioral effects among workers with chronic mine whether deficits in olfactory function process changes have occurred in this industry
low-level fumigant exposure.5 Sulfuryl fluo- are present in other sulfuryl fluoride-exposed over the last several decades, suggesting that
ride-exposed workers had nonsignificantly populations and whether these deficits repre- fumigant exposure has not changed over the

1778 American Journal of Public Health December 1998, Vol. 88, No. 12
Health Effects Among Structural Fumigation Workers

TABLE 4-Multiple Linear Regression Results Comparing Performance on Neurobehavioral Tests, the UPSIT, and the
Contrast Sensitivity Test Among Structural Fumigation Workers With High Methyl Bromide Exposure or High
Sulfuryl Fluoride Exposure During the Year Preceding Examination vs Unexposed Referentsa: South Florida,
1992-1 993
Workers With High Methyl Workers With High Sulfuryl
Bromide Exposure Over the Year Fluoride Exposure Over the Year
Preceding Examination (n = 28) Preceding Examination (n = 91)
Direction of Workers With High Direction of Workers with High
Methyl Bromide Exposure Sulfuryl Fluoride Exposure
Test Compared With the Referent Groupb P Compared With the Referent Groupb p
Hand-Eye Coordination + .70 + .73
Simple Reaction Time .37 + .48
Continuous Performance Test: response time + .62 - .93
Continuous Performance Test: NR + .70 + .11
Symbol Digit .83 - .89
Symbol Digit Recall score .51 + .91
Pattern Memory + .54 - .05
Pattern Memory recall time .45 - .17
Serial Digit Learning score + .27 + .70
Mood Scale Score: anger + .72 - .47
Mood Scale Score: confusion + .13 - .73
Mood Scale Score: depression + .62 - .57
Mood Scale Score: fatigue + .80 - .75
Mood Scale Score: tension + .86 - .74
Santa Ana: preferred hand .22 - .03
Santa Ana: nonpreferred hand .71 - .58
UPSIT (no. correct/40) + .21 - .03
UPSIT, % + .67 - .05
Contrast sensitivity: right eye .67 + .86
Contrast sensitivity: left eye + .95 + .64
Note. UPSIT= University of Pennsylvania Smell Identification Test; NR = nonresponses.
aWorkers with high methyl bromide exposure and high sulfuryl fluoride exposure are defined as workers who used each substance on 50% or
more of jobs. Models for the computerized neurobehavioral tests controlled for age, years of education, and test language (English or
Spanish). Models for the Santa Ana Dexterity Tests controlled for age and race. Models for UPSIT controlled for smoking status (current
smoker, former smoker, never smoker), years of education, and race. Models for contrast sensitivity controlled for age, acuity of the
examined eye, and years of education.
+= Performance of fumigation workers was better vs referents based on adjusted means. - = Performance of fumigation workers was worse
vs referents based on adjusted means.

last several years. It is unlikely that our find- differences were found between the examined exposure may be associated with adverse
ings are limited by inaccurate exposure esti- and refusant workers for these variables effects on olfactory function and some cog-
mates provided by the workers. The exposure (results not shown). nitive functions. Few health effects were
estimates used in this study had adequate Other potential limitations may be pres- associated with methyl bromide exposure,
agreement with exposure estimates obtained ent. Using friends and neighbors as controls possibly because this study had limited
from company records.9 may bias findings toward the null or in the power to assess this exposure. D
Many of the fumigation workers (63%) opposite direction.28 There are also limitations
and referents (41%) were also exposed to due to the cross-sectional design (e.g., tempo- Acknowledgments
other pesticides at work or home. These pesti- ral sequence of cause and effect, and inclusion We thank several who assisted with the study from
cides included chlorpyrifos, organophos- of only workers currently employed in the NIOSH (Bill Ehling, Kim Jenkins, Marian Coleman),
phates, carbamates, pyrethrins, and organo- fumigation industry). Finally, all but 11 fumi- the University of Miami (Chris Hubbard, Dr Joel
chlorines. We found that the pattern memory gation workers were exposed to both methyl Glaser, Bruce Mann, Maria Bizzio, Dr Judy Bean,
Gabriela Ramirez, Marta Bustillo, Guadelupe Bay-
test and olfactory tests were not significantly bromide and sulfuryl fluoride (the 11 were ona, Tony Bolet), and Biotrax (Nada Elmore, Jean
associated with any of these classes of pesti- exposed to sulfuryl fluoride only). These con- Wilhite, Patrick Koenig, Beth Honchell). We also
cides. In addition, chloropicrin is not known comitant exposures may have limited our thank the participating fumigation companies for
to produce neurotoxicity. This information ability to distinguish between methyl bromide their assistance in recruiting study participants.
suggests that none of these pesticide classes or and sulfuryl fluoride effects. Despite these
chloropicrin is responsible for the findings limitations, this is the largest known study References
observed in this study. examining neurological function among 1. Environmental Protection Agency. Protection of
Participation bias is unlikely to be workers exposed to these fumigants. stratospheric ozone: supplemental rule to amend
responsible for our findings. Of 24 workers In conclusion, this study found some phaseout of ozone-depleting substances to
who declined to participate, 18 (75%) agreed health effects associated with employment in include potential production allowances for
the structural fumigation industry. The methyl bromide, Federal Register (1994) (codi-
to be interviewed by telephone. These indi- fied at 40 CFR Part 82).
viduals were asked questions similar to those peripheral nerve effects were most likely 2. Alexeeff GV, Kilgore WW. Methyl bromide.
from the full study, including questions on associated with adverse ergonomic factors Residue Rev. 1983;88:101-153.
age, race, years employed in the fumigation experienced by tent crew workers. In addi- 3. Verberk MM, Rooyakkers-Beemster T, De
industry, and current job title. No significant tion, this study found that sulfuryl fluoride Vlieger M, Van Vliet AGM. Bromine in blood,

December 1998, Vol. 88. No. 12 American Journal of Public Health 1779
Calvert et al.

TABLE 5-Multiple Linear Regression Results Comparing Performance on Neurobehavioral Tests, the UPSIT and the
Contrast Sensitivity Test Among Structural Fumigation Workers vs Unexposed Referents: South Florida,
1992-1993

Fumigation Worker Referent Direction Worse Performance With


Adjusted Adjusted P for Adjusted of Worker Increasing Duration of
Test n Meana n Meana Analysis Performanceb Fumigant Exposurec
Hand-Eye Coordination, rmse 118 2.21 116 2.22 .76 +
Simple Reaction Time, ms 118 265.4 116 265.3 .99
Continuous Performance Test: 118 399.3 116 397.0 .66 - MB
response time, ms
Continuous Performance Test: NR 118 0.47 116 0.73 .19 +
Symbol Digit, s/digit 118 2.26 116 2.24 .82 -
Symbol Digit Recall score 118 4.67 116 4.75 .81 -
Pattern Memory, % 118 84.9 116 87.3 .12 - SF
Pattern Memory recall time, s 118 6.26 116 5.93 .15 - MB, SF
Serial Digit Learning score 118 4.61 116 5.09 .40 +
Mood Scale Score: anger 118 1.88 116 1.83 .58 - SF
Mood Scale Score: confusion 118 2.27 116 2.26 .92 -
Mood Scale Score: depression 118 1.89 116 1.83 .56 -
Mood Scale Score: fatigue 118 2.63 116 2.60 .82 -
Mood Scale Score: tension 118 2.40 116 2.35 .67 -
Santa Ana: preferred hand 121 39.9 120 41.5 .02 - SF
Santa Ana: nonpreferred hand 121 36.9 120 37.4 .50 - SF
UPSIT (no. correct/40) 109 33.6 106 34.5 .11 - SF
UPSIT, % 123 82.8 120 85.1 .10 - SF
Contrast sensitivity: right eye 121 12.2 120 12.2 .83 +
Contrast sensitivity: left eye 122 12.2 119 12.1 .69 +
Note. UPSIT = University of Pennsylvania Smell Identification Test; rmse = root mean square error; NR = nonresponses.
aModels for the computerized neurobehavioral tests controlled for age, years of education, and test language (English or Spanish). Models for
the Santa Ana Dexterity Tests controlled for age and race. Models for UPSIT controlled for smoking status (current smoker, former smoker,
never smoker), years of education, and race. Models for contrast sensitivity controlled for age, acuity of the examined eye, and years of
education.
b+= Performance of workers was better vs referents based on adjusted means. - = Performance of workers was worse vs referents based on
adjusted means.
cSF = based on adjusted analyses, as sulfuryl fluoride exposure increased (referent, low sulfuryl fluoride years of exposure, high sulfuryl
fluoride years of exposure), monotonically decreasing performance was observed.
MB = based on adjusted analyses, as methyl bromide exposure increased (referent, low methyl bromide years of exposure, high methyl
bromide years of exposure), monotonically decreasing performance was observed.

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1780 American Journal of Public Health December 1998, Vol. 88, No. 12

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