See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/6722900

Chronic bronchitis and pesticide exposure: A case-control study in Lebanon

Article  in  European Journal of Epidemiology · November 2006

DOI: 10.1007/s10654-006-9058-1 · Source: PubMed

CITATIONS READS

26 528

5 authors, including:

Pascale Salameh Mirna Waked

Lebanese University Saint George Hospital University Medical Center
605 PUBLICATIONS   4,889 CITATIONS    99 PUBLICATIONS   1,221 CITATIONS   

SEE PROFILE SEE PROFILE

Patrick Brochard Bernadette Abi Saleh

University of Bordeaux Sagesse University
398 PUBLICATIONS   5,701 CITATIONS    10 PUBLICATIONS   439 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Antibiotics use in Lebanon View project

Safe Handling Of Cytotoxic Drugs View project

All content following this page was uploaded by Pascale Salameh on 22 December 2013.

The user has requested enhancement of the downloaded file.

European Journal of Epidemiology (2006)
Springer 2006
DOI 10.1007/s10654-006-9058-1

Chronic bronchitis and pesticide exposure: a case–control study in Lebanon

Pascale R. Salameh1, Mirna Waked2, Isabelle Baldi3, Patrick Brochard3 and Bernadette Abi
Saleh1
1
Faculty of Public Health, Lebanese University, Beirut, Lebanon; 2Faculty of Medicine, Balamand University, El-Koura,
Lebanon; 3Faculty of Public Health, ISPED, Victor Segalen Bordeaux 2 University, Bordeaux, France

Received: 19 April 2006/Accepted in revised form 25 August 2006

Abstract. Objective Pesticides are widely used toxics.
The objective of the study is to evaluate the odds of
exposure to pesticides in chronic bronchitis patients.
Methods Using the American Thoracic Society stan-
dardized questionnaire confirmed by medical diag-
nosis of chronic bronchitis, a case–control study
was performed in Lebanon. Pesticide exposure was
estimated and between groups comparison was made.
Results The study involved 262 controls and 110
chronic bronchitis outpatient subjects from 10 medical
centers. Any exposure to pesticides was associated to
chronic bronchitis (OR = 2.46 [1.53–3.94]; p < 10)4).
Occupational use presented the highest association
(15.92 [3.50–72.41]; p < 10)4), followed by regional
exposure (3.70 [2.05–6.70]; p < 10)4). Results were
confirmed by multivariate and subgroup analysis.
Conclusion Pesticide exposure was associated with
chronic bronchitis in Lebanese adults. Pesticides tox-
icological effects may explain chronic respiratory ef-
fects associations found with all exposure types.

Key words: Chronic bronchitis, Non-Occupational Exposure, Occupational Exposure, Pesticides, Respiratory
Symptoms

Introduction environmental health concern [14]. In Nicaragua, a

Symptoms related to chronic bronchitis have been
reported in agricultural workers [1]: these may be
systemic effects on lungs after inhalation, rather than
direct local effects, and at doses much lower to those
causing similar responses after dermal or oral expo-
sure [2].
Inhalation of pesticides at the worksite is notice-
able [3]. Farming and agricultural work were associ-
ated with several respiratory problems such as
asthma and chronic obstructive pulmonary disease
[4–6], and pesticides were cited as possible causing
factors [7]. Occupational exposure to pesticides has
been associated with respiratory symptoms and
chronic respiratory diseases such as asthma [8].
In addition, many indirect and direct exposure
opportunities exist for farmers’ next of kin who live in
places where pesticides are used or brought home by
lack of decontamination measures [9, 10]. Subjects
living in heavily treated regions are further exposed to
pesticide air pulverization and contaminated food and
water [11, 12]. The general population is also exposed
to pesticides by domestic use or accidental exposure.
Non-occupational chronic respiratory indoor expo-
sure can result in high annual cumulative doses [13].
Little is known about the health effects of nonoccu-
pational pesticide exposure, but living in areas
where pesticides are used on crops may represent an
strong association has been found between living in a
highly pesticide treated region and frequency increase
of various intoxication symptoms [15].
In Lebanon, statistics regarding pesticides acute or
chronic intoxication do not exist yet [16]; pesticides of
all types are used (organophosphates, pyrethroids...),
except for some that have been banned all over the
world. More than 50% of acute intoxication cases
may be due to occupational use of pesticides during
treatment season, in parallel to mild and chronic
intoxications [17]. We have previously studied the
effects of pesticides on asthma in children [18] and
adults [19], both showing positive associations, con-
firmed by quantitative and multivariate analyses.
However, nothing is known about the effects of pes-
ticides on chronic bronchitis.
The objective of this study is thus to evaluate the
odds of occupational, domestic or environmental
exposure to pesticides in chronic bronchitis adults in
Lebanon, in comparison with controls.
Methods
Study design
We conducted a case control study, comparing pes-
ticide exposure in new outpatient cases of chronic
bronchitis, and in controls without respiratory
problems. Chronic bronchitis represented the
dependent variable, pesticide exposure the indepen-
dent one, and potential confounding variables the
covariates.
Population of the study
Cases and controls were recruited in 10 out of 148
(6.76%) Lebanese hospital centers, chosen from the
list of hospitals according to convenience in all Leb-
anese regions: three in Beirut, four in Mount Leba-
non, one in Northern Lebanon, one in the Bekaa, and
one in Southern Lebanon.
Procedure
One pulmonologist was contacted within every hos-
pital, leading to 10 pulmonologists participating to
the study: this allows for an average ratio of 1
pneumonologist/4 · 105 Lebanese inhabitants. After
they agreed to contribute to the study, they were
asked to recruit cases of newly diagnosed chronic
bronchitis outpatients, with or without obstruction.
Any other chronic pulmonary pathology diagnosed
by pulmonologists was an exclusion criterion
(tuberculosis, fibrosis, cancer...); asthma patients
were included in the study, but not in this analysis.
Participants aged between 12 and 99 years were in-
cluded in the study.
Controls were taken from a source population of
individuals accompanying cases (parents, friends) or
seeking advice for another problem in the same
hospital, also as outpatients. Any disease regarding
gastroenterology, endocrinology, orthopedics, cardi-
ology, surgery, neurology, nephrology, and urology
specialties could be an inclusion criterion for con-
trols. However, any chronic respiratory symptom or
problem reported by controls before filling in the
questionnaire was an exclusion criterion.
Information was given to responders consisting of
‘‘a questionnaire regarding their health, the results of
which will be useful for science’’. They orally con-
sented to give the required information.
A pretested self administered questionnaire [20],
adapted to local arabic language from the standard-
ized and validated American Thoracic Society
chronic respiratory disease questionnaire [21], was
given to pulmonologists, to administer to any subject
fulfilling inclusion criteria. Questionnaires were
delivered to eligible subjects by local inquirers, inde-
pendently of exposure status. The same conditions
were applied for questionnaires in both cases and
controls, to evaluate the diagnosis, in addition to
occupational, regional, local and domestic pesticides
exposures.
Analysis
The dependent variable ‘‘chronic bronchitis’’ was
defined according to guidelines for clinical definition
of chronic bronchitis: daily productive cough for
3 months or more per year, over 2 consecutive years
or more [22]. In addition to the pulmonologist diag-
nosis, reported symptoms in the self-administered
questionnaire allowed to study the declared chronic
bronchitis issue.
The presence of symptoms was indicated in the
questionnaire by affirmative responses to the ques-
tions, ‘‘Do you usually have cough first thing in the
morning?’’ ‘‘Do you bring up phlegm from the chest
in the morning?’’ Concordance between the answers
to the questionnaire and the pulmonologists’ diag-
nosis was confirmed by an independent pulmonol-
ogist. Only in this case was the individual classified
as a case. In case of discordance, the individual was
removed from the analysis. Classification into a
control required a double absence of diagnosis and
of positive answers to the respiratory symptoms’
questions.
For pesticide exposure, questions were the
following ones: ‘‘Have you ever used pesticides in
your work?’’ ‘‘Have you ever used pesticides out of
your work (for house or garden treatment...)?’’ ‘‘Do
you live in a region heavily treated by pesticides?’’
‘‘Do you live in the proximity of a heavily treated
field by pesticides?’’... An expert in agronomy, who
assigned to residency regions a score from 0 to 9
according to yearly consumption of pesticides,
provided complementary evaluation of regional
exposure. Personal occupational pesticide exposure,
occupational use by a family member, regional
exposure due to residence in a heavily treated
region (score >4) or local exposure due to prox-
imity to a heavily treated field, personal non
occupational exposure by personal house or garden
treatment, and exposure by house treatment by
someone else, were evaluated. A variable named
‘‘ever exposed’’ is considered positive if the subject
declared any exposure type. Cumulative exposure
indices were also calculated: one as the product of
region score by the number of years of residence in
the region, and another as the number of yearly
uses by the number of years of use when applica-
ble. Questions related to the types of pesticides
used were eliminated since the majority of respon-
dents were unable to answer them.
Education level was quantified according to the
number of years of scholarization. Active smoking
was determined by several questions, categorizing
subjects in non-smokers (smoking history of less
than 20 packs in a lifetime), current smokers, and
ex-smokers. The number of pack-years was deter-
mined by multiplying the average number of packs
of 20 cigarettes smoked per day by the number of
years of smoking. Passive smoking was character-
ized by the number of smokers at home. Working in
dusty and smoky environments were also asked
about.
Data analysis was performed on SPSS software
(version 12.0). Two-sided statistical tests were used;
v2 test for dichotomous or multinomial qualitative
variables, Fisher exact two-sided test in case of
expected counts in cells <5, Mann–Whitney or
Wilcoxon test for quantitative variables with non-
homogeneous variances and non normal distribu-
tion, and Students’ t-test for quantitative variables
of normal distribution and homogeneous variances.
In cumulative exposure indexes, a trend test was
used to evaluate the OR increase in case of increase
in exposure intensity or duration.
Regarding multivariate analysis, a descending
stepwise likelihood ratio logistic regression was
performed. Adjustment over all potential con-
founding variables, showing baseline difference be-
tween the groups of comparison ( p < 0.20), was
done: number of tobacco pack-years, number of
smokers at home, sex, age, education, residency
department, hospital, body mass index, allergy,
nationality, working in a smoky and in a dusty
environment, personal cardiac and paternal respi-
ratory problem history were included in the analy-
sis.
Sample size calculation was performed with an
alpha risk of 5%, a beta risk of 20%, and a minimal
exposure probability of 30%, representing half the
percentage of Lebanese exposed to pesticides [21].
The minimal sample size necessary to show a twofold
increase in risk consisted of 339 subjects, divided as 2
controls for 1 case.
Results
About 790 questionnaires (53%) were filled in out of
1500 distributed; 33 were then eliminated because of
inadequate filling; 757 were accepted (50%).
About 140 (27.8%) subjects reported symptoms not
in accordance with medical diagnosis and presented
unclassifiable respiratory problems: these individuals
either had some respiratory symptoms, but their
frequency or duration was not in accordance with the
chronic bronchitis definition, or suffered from
chronic respiratory symptoms while they were not
diagnosed by the pulmonologist as cases. In addition,
245 (32.4%) presented asthma [19]. The former and
the latter categories were not included in the analysis.
About 372 questionnaires were finally analyzed. Re-
sults are presented for these 110 (29.6%) chronic
bronchitis patients and 262 controls (70.4%).
Social and demographic characteristics
Social and demographic characteristics are summa-
rized in able 1. Male sex, lower educational level, and
non Lebanese nationality were more common in
cases than in controls; the former had also higher
body mass index ( p < 0.05) (Table 1).
Smoking, toxics and dust exposure, medical and family
history
Cases were more frequently active present or past
smokers, with a higher cumulative smoking exposure.
There were more smokers in the house of cases than of
controls. There were also more workers in dusty and
toxic gases environments and cardiac problems
(Table 2).

Table 1. Social and demographic characteristics

Variable Controls N = 262 (%) Cases N = 110 (%) p-value

Department 0.09a
Beirut 34 (13.0%) 17 (15.5%)
Mount Lebanon 149 (57.1%) 48 (43.6%) 0.19b
South Lebanon 11 (4.2%) 11 (10.0%) 0.18b
North Lebanon 47 (18.0%) 24 (21.8%) 0.96b
Bekaa 20 (7.7%) 10 (9.1%) 0.81b
Age in years M(SD) 37.6 (14.9) 50.7 (15.6) <10)4
Sex
Male 116 (44.3%) 72 (65.5%) <10)3
Female 146 (55.7%) 38 (34.5%)
Education level <10)4a
<9 years 41 (16.0%) 51 (46.3%)
9 years or more 95 (37.0%) 19 (17.3%) <10)4b
College graduate 121 (47.1%) 51 (21.1%) <10)4b
Nationality
Non Lebanese 2 (0.8%) 7 (6.4%) 0.003
Lebanese 259 (99.2%) 102 (93.6%)
BMIc M(SD) 24.4 (3.8) 26.7 (4.2) <10)4
a
p-value for the whole distribution; bp-value for every stratum against first cited stratum; cBMI = Body Mass Index,
calculated by BMI = weight in kg /(height in m)2.
Table 2. Smoking status, toxic exposure, personal disease and family history

Variable Controls Cases p-value

N = 262 (%) N = 110 (%)

Smoking status <10)6a

Non smoker 178 (67.9%) 15 (13.6%)
Previous smoker 34 (13.0%) 31 (28.2%) <10)8b
Actual smoker 52 (19.9%) 64 (58.2%) <10)8b
Pack-years 3.11 (8.53) 28.4 (28.9) <10)4
Smokers at home <10)4a
No smoker 123 (47.3%) 19 (18.3%)
1 smoker 59 (22.7%) 25 (24.0%) 0.003b
More than one 78 (30.0%) 60 (57.7%) <10)8b
Works in a smoky place 4 (1.5%) 9 (8.4%) 0.003
Works in a dusty place 24 (9.2%) 24 (22.4%) 0.001
Chest trauma 7 (2.7%) 4 (3.6%) 0.62
Cardiac disease 10 (3.8%) 19 (17.3%) <10)4
Allergy 33 (12.6%) 21 (19.1%) 0.11
Paternal respiratory problem 9 (3.4%) 8 (7.3%) 0.11
Maternal respiratory problem 21 (8.0%) 11 (10.0%) 0.53
a
p-value for the whole distribution; bp-value for every stratum against first cited stratum.

Table 3. Pesticides exposure types and chronic bronchitis in Lebanon

Exposure type Controls Cases OR [95% CI]

N = 262 (%) N = 110 (%)

Any exposure 123 (47.3%) 75 (68.8%) 2.46 [1.53–3.94]

Occupational 2 (0.8%) 12 (10.9%) 15.92 [3.50–72.41]
exposure
Non occupational 68 (26.0%) 52 (47.3%) 2.56 [1.61–4.07]
exposurea
House exposureb 73 (27.9%) 41 (37.3%) 1.54 [0.96–2.47]
Regional exposurec 24 (9.2%) 30 (27.3%) 3.70 [2.05–6.70]
Local exposured 34 (13.0%) 30 (27.3%) 2.50 [1.44–4.35]
Paraoccupational 9 (3.4%) 5 (4.6%) 1.35 [0.44–4.13]
exposuree
a
Personal non occupational use of pesticides; bHouse treated by pesticides; cLives in a region heavily treated by pesticides;
d
Lives near a field heavily treated by pesticides; ea family member is occupationally exposed to pesticides.

Exposure to pesticides and chronic bronchitis
Types of pesticides exposure are reported in Table 3,
with all associations statistically significant, except
for paraoccupational use. Any exposure to pesticides
was associated with chronic bronchitis: occupational
use presented the highest association, while indirect
exposure by house treatment was the least associated.
Multivariate analysis
Stepwise descending likelihood ratio logistic regres-
sions were performed. Variables retained in the final
model were number of tobacco pack-years, educa-
tion, nationality, and passive smoking; on the con-
trary, other introduced variables such as age, sex,
hospital, residency department, body mass index,
allergy, personal and paternal respiratory problem
did not fit adequately in the model, and were subse-
quently removed. Adjusted ORs demonstrated sig-
nificant correlations of exposure to pesticides and
chronic bronchitis, with higher associations for all
types of exposure (Table 4). In the multiple exposure
model, professional use and house exposure variables
lost significant associations with chronic bronchitis,
while personal non occupational, local and regional
exposure were still significantly correlated to chronic
bronchitis, along with active and passive smoking
(Table 4).
Quantitative exposure analysis
Cumulative exposure classes showed that there is a
significant increase in the risk of chronic bronchitis
with the increase in intensity and/or duration of dif-
ferent levels of exposure to pesticides (Table 5).
Table 4. Pesticides exposure and chronic bronchitis in Lebanon – multivariate analysis

Variable Adjusted Significant factors

OR [95% CI] retained in the modelsa

Any exposure 5.05 [2.19–11.63] Education, nationality,

number of tobacco pack-years,
number of smokers at home
Occupational exposure 8.85 [1.15–66.67] Education, nationality,
number of tobacco pack-years,
number of smokers at home
Non occupational 3.79 [1.77– 8.13] Education, nationality,
exposureb number of tobacco pack-years
House exposurec 4.92 [2.26–10.75] Education, nationality,
number of tobacco pack-years
Regional exposured 6.06 [2.46–16.67] Education, nationality,
number of tobacco pack-years,
number of smokers at home
Local exposuree 3.62 [1.59– 8.19] Education, nationality,
cumulative active smoking
Multiple exposure model
Occupational exposure 2.05 [0.28–14.91] Number of tobacco pack-years,
Non occupational 4.39 [1.87–10.27] number of smokers at home
exposureb
House exposurec 1.62 [0.54–4.90]
Regional exposurec 13.91 [2.77–69.79]
Local exposured 8.33 [1.37–50.00]
a
Adjustment was over number of tobacco pack-years, number of smokers at home, sex, age, education, residency depart-
ment, hospital, body mass index, allergy, nationality, working in a smoky and in a dusty environment, personal cardiac and
paternal respiratory problem history; bPersonal non occupational use of pesticides; cHouse treated by pesticides; dLives in a
region heavily treated by pesticides; eLives near a field heavily treated by pesticides.

Subgroup analysis eventually, chronic pulmonary obstruction. In the

In Table 6, data is presented for multivariate analysis
in two subgroups: non smokers and ever smokers.
Associations found between chronic bronchitis and
pesticides exposure seemed even stronger in non
smokers compared with smokers, except for regional
exposure.
Discussion
In this Lebanese case–control study on chronic
bronchitis, we found a moderate to strong correlation
between exposure to pesticides and this disease.
The correlation was the strongest for occupational
exposure. Dose effects relationship and multivariate
analysis confirmed the results obtained in bivariate
analysis, by taking into account potential confound-
ing variables. The relative imprecise estimates and
borderline significance in cumulative occupational
exposure association with chronic bronchitis and in
subgroup analysis is probably due to the small
number of individuals in that category. House
application of pesticides does not seem to be an
independent risk factor for chronic bronchitis.
Several epidemiological and toxicological studies
have shown results comparable to those of the current
study, regarding chronic respiratory symptoms, and
Iowa Farm Family Health and Hazard Surveillance
Project, among farmers, applying pesticides to live-
stock was associated with significantly increased odds
of phlegm (OR = 1.91; 95% CI 1.20–3.57), chest ever
wheezy (OR = 3.92, 95% CI 1.76–8.72), and flu-like
symptoms (OR = 2.93, 95% CI 1.69–5.12) in models
adjusting for age and smoking [7]. In an epidemio-
logical study on grapes and apple trees workers,
excessive chronic respiratory symptoms have been
found: dyspnea and suffocation crisis (74.1% vs.
5.2%), cough (27.6% vs. 15.7%), expectoration (25.3%
vs. 13.8%) and chronic bronchitis (20.7% vs. 13.9%),
and also acute symptoms in smokers of more than
10 years employment duration. Low respiratory vol-
umes (0.54 vs. 0.73 in FVC measured-predicted dif-
ference, and 0.12 vs. 0.35 in FEV1 measured-predicted
difference) were noted even after adjustment for
smoking, suggesting obstructive and restrictive effects.
Pesticides were suggested as contributing agents to all
of these effects [1].
For regional exposure, several accidents occurred,
where people living next to fumigant treated surface
(most toxic pesticides used in agriculture) [11] expe-
rienced laryngeal irritation, headache, or acute pul-
monary irritation, cough and even death [23]. With
paraquat, several symptoms were reported such as
cough, rhinitis, dyspnea, wheezing... [24]. However,
no other study explicitely reported the association
Table 5. Mean cumulative exposure to pesticides and chronic bronchitis in Lebanon

Cumulative exposure Controls Cases OR Trend

N = 262 N = 110 [95% CI] test p-value

Occupational exposure 0.001

0 application 260 (72.6%) 98 (27.4%) 1
3–10 applications 0 3 (100%) Undetermined
11–30 applications 0 1 (100%) Undetermined
>30 application 0 3 (100%) Undetermined
Non occupational exposurea <10–4
<1 application 194 (77.0%) 58 (23.0%) 1
1–6 applications 9 (60.0%) 6 (40.0%) 2.23
7–24 applications 9 (52.9%) 8 (47.1%) 2.97
>24 applications 2 (15.4%) 11 (84.6%) 18.4
House exposureb 5E-04
<12 applications 189 (73.3%) 69 (26.7%) 1
12–31 applications 30 (83.3%) 6 (16.7%) 0.55
32–47 applications 25 (69.4%) 11 (30.6%) 1.21
>47 applications 18 (42.9%) 24 (57.1%) 3.65
Weighted regional exposurec 0.003
<3 years 56 (66.7%) 28 (33.3%) 1
3–77 years 48 (80.0%) 12 (20.0%) 0.5
78–186 years 50 (80.6%) 12 (19.4%) 0.48
> 186 27 (44.3%) 34 (55.7%) 2.52
Local exposured 0.002
<1 year 227 (73.9%) 80 (26.1%) 1
1–10 years 12 (60.0%) 8 (40.0%) 1.89
11–25 years 8 (50.0%) 8 (50.0%) 2.84
>25 years 8 (44.4%) 10 (55.6%) 3.55
a
Lifetime personal non occupational use of pesticides; bLifetime house treatments by pesticides; cDuration of living in a
region heavily treated by pesticides multiplied by the intensity code for use of pesticides in that region; dDuration of living
near a field treated by pesticides.

Table 6. Pesticides exposure and chronic bronchitis in Lebanon – subgroup analysis

Exposure type Smokers Non smokers

ORa [95% CI] ORa [95% CI]

Any exposure 3.92 1.28–12.05 6.92 1.90–25.19

Occupational exposure 3.68 0.32–41.67 12.50 0.63–2.50
Non occupational exposurea 4.85 1.45–16.29 14.20 4.20–47.99
House exposureb 4.10 1.26–13.33 6.99 2.14–22.73
Regional exposurec 9.52 1.64–55.56 4.24 1.20–14.93
Local exposured 3.60 1.09–11.90 3.53 0.98–12.66
ORa = Adjusted Odds
Ratio; aPersonal non occupational use of pesticides; bHouse treated by pesticides; cLives in a region
heavily treated by pesticides; dLives near a field
heavily treated by pesticides.

between chronic bronchitis and non occupational use
of pesticides.
Biological plausibility of our results is confirmed
by multiple experimental toxicological studies on
animals, in addition to known clinical effects of
high level exposure, such as by organophosphates or
pyrethroids [2, 22]. Besides hypersensitivity, the
development of the respiratory problems is mainly
due to overwhelming of detoxification capacity of
cells [2]: activation and detoxification balance play a
determinant role in defining pesticide toxicity [25].
Difference in strength of associations between the
subgroups of smokers and non smokers could be
explained by the toxicokinetic interaction between
smoking and pesticides. Cigarette smoke contains
polycyclic hydrocarbons, which are well known
inducers of hepatic mixed function oxidases [26]; on
the other hand, several pesticides are metabolized
by similar liver cytochromes [27–29]. Smokers may
thus be able to metabolize pesticides at a higher rate
than non smokers [30], and may not be as affected
by their toxic effects as non smokers. This issue
remains to be further explained by larger scale
studies.
It was not possible to get detailed information on
non responders, and we assumed that the main rea-
sons for refusal would only be either illiteracy or non
motivation, since subjects were unaware of the exact
objective of the study. Moreover, pulmonologists
recruiting subjects were unaware of their exposure
status, especially when considering various types of
exposure (regional, occupational, domestic,...).
On the other hand, we assume that our results
underestimate the association between pesticide
exposure and chronic bronchitis for several reasons.
The geographical comparability of cases and controls
and the fact that family members were sometimes
taken as controls may cause them to have similar non
occupational exposures to pesticides. In addition,
despite the use of a validated questionnaire, recall
bias may be possible because information on expo-
sure was based on self-report without further evalu-
ation, but it is most probably a non differential one
between the two groups of comparison since both
groups were unaware of the exact objectives of the
study. Furthermore, controls were persons who
would become cases, were they to develop the disease,
because of similar conditions of selection in the hos-
pitals; however, their mixed diagnosis make them non
comparable to the general population, and induce an
underestimation of the expected associations. Resid-
ual confounding is also possible, because it was not
possible to take into account farming environment
toxics other than pesticides and other pollutants.
Specific dosing studies would be required to solve
these issues.
In conclusion, we can say that in our study pesti-
cide exposure was associated with chronic bronchitis
in adults. The observed effects cannot be related to a
specific pesticide since several products are used
concomitantly or vary with time, season, crops type,
and personal preference. Air monitoring of different
pesticides and other pollutants concentrations would
be necessary in future research to confirm the present
results.
References
1. Zuskin E, Mustajbegovic J, Neil Schachter E, Kern J,
Pavicic D. Respiratory function in vineyard and orch-
ard workers. Am J Ind Med 1997; 30: 250–255.
2. Dinsdale D. Pulmonary toxicity of anticholinesterases.
In: Ballantyne B, Mans TC (eds), Clinical and Experi-
mental Toxicology of Organophosphates and Carba-
mates. Butterworth Heinemann Editor, 1992: 156–166.
3. American Thoracic Society. Respiratory health hazards
in agriculture. Am J Respir Crit Care Med 1998; 158:
S1–S76.
4. Choma D, Westeel V, Dubiez A, et al. Respective
influence of occupational and personal factors on
respiratory function in dairy farmers. Rev Mal Resp
1998; 15(6): 765–772.
5. Dalphin JC, Dubiez A, Monnet E, et al. Prevalence of
asthma and respiratory symptoms in dairy farmers in
the French province of the Doubs. Am J Resp Crit
Care Med 1998; 158(5pt1): 1493–1498.
6. Dalphin JC. Chronic obstructive bronchitis in a fodder
farming setting. Rev Mal Resp 1996; 13(6): 575–581.
7. Sprince NL, Lewis MQ, Whitten PS, Reynols SJ,
Zwerling C. Respiratory symptoms: associations with
pesticides, silos and animal confinement in the Iowa
farm family health and hazard surveillance project. Am
J Ind Med 2000; 38(4): 455–462.
8. Senthilselvan A, Mcduffie H, Dosman J. Association of
asthma with use of pesticides. Am Rev Respir Dis 1992;
146: 884–887.
9. Fenske R. Pesticides exposure assessment of workers
and their families. Occup Med 1997; 12(2): 221–237.
10. Gladen BC, Sandler DP, Zahm SH, Kamel F, Rowland
AS, Alavanja MC. Exposure opportunities of families
of farmer pesticide applicators. Am J Ind Med 1998;
34(6): 581–587.
11. Moses M. Pesticide-related health problems and farm
workers. AAOHN J 1989; 37(3): 115–130.
12. Al-Saleh I. Pesticides: a review article. J Environ Pathol
Toxicol Oncol 1994; 13(3): 151–161.
13. Whitmore R, Immerman F, Camann D, Bond A, Lewis
R, Schaum J. Non-occupational exposures to pesticides
for residents of two U.S. cities. Arch Environ Contam
Toxicol 1994; 26: 47–59.
14. Azaroff LS, Neas LM. Acute health effects associated
with non occupational pesticide exposure in rural El
Salvadore. Environ Res 1999; 80(2pt1): 158–164.
15. Keifer M, Rivas F, Moon JD, Checkoway H. Symp-
toms and cholinesterase activity among rural residents
living near cotton fields in Nicaragua. Occup Environ
Med 1996; 53(11): 726–729.
16. Chatila S. A Brief Report On An Environmental
Problem in Lebanon: ‘‘Pesticides’’. Beirut: AUB pub-
lications, 1996.
17. Trabulsi A. Pollution des aliments et cultures traités
par les pesticides. Beirut: Conférence de l’homme et de
l’environnement, 1991.
18. Salameh P, Baldi I, Brochard P, Raherison C, Abi Saleh
B, Salamon R. Respiratory symptoms in children and
exposure to pesticides. Eur Resp J 2003; 22: 507–512.
19. Salameh P, Waked M, Baldi I, Brochard P, Abi Saleh
B. Asthma and pesticide exposure: a case–control study
in Lebanon. J Epidemiol Commun Health 2006; 60(3):
256–261.
20. Salameh P. Acts of the First Franco-Lebanese Envi-
ronment and Health Congress. Beirut: Faculty of
Health Sciences Publications – Lebanese University,
1999, 160 pp–164.
21. Ferris BG. Epidemiology standardization project. Am
Rev Resp Dis 1978; 118: 1–88.
22. Pauwels RA, Buist AS, Ma P, Jenkins CR, Hurd SS.
GOLD scientific committee. Global strategy for the
diagnosis, management, and prevention of chronic
obstructive pulmonary disease: National Heart, Lung,
and Blood Institute and World Health Organization
global initiative for chronic obstructive lung disease
(GOLD) executive summary. Resp Care 2001; 46: 798–
825.
 23. Ecobichon D. Toxic effects of pesticides. In: Curtis D.
Klaassen (ed), Casarett & Doull’s toxicology: the basic
science of poisons. McGraw-Hill edition, USA, 1996;
643–689.
24. Ames R, Howd R, Doherty L. Community exposure to
paraquat drift. Arch Environ Health 1993; 48(1): 47–51.
25. Witschi H, Last J. Toxic responses of the respiratory
system. In: Curtis D. Klaassen (ed) Casarett & Doull’s
toxicology: the basic science of poisons. McGraw-Hill
edition, USA, 1996; 443–462.
26. Alvares AP. Research review. Interactions between
environmental chemicals and drug biotransformation
in man. Clin Pharmacokinet 1978; 3(6): 462–477.
27. Rose RL, Tang J, Choi J, et al. Pesticide metabolism in
humans, including polymorphisms. Scand J Work
Environ Health 2005; 31(Suppl 1): 156–163.
28. Sams C, Cocker J, Lennard MS. Biotransformation of
chlorpyrifos and diazinon by human liver microsomes
View publication stats
and recombinant human cytochrome P450s (CYP).
Xenobiotica 2004; 34(10): 861–873.
29. Burim RV, Canalle R, Martinelli Ade L, Takahashi
CS. Polymorphisms in glutathione S-transferases
GSTM1, GSTT1 and GSTP1 and cytochromes P450
CYP2E1 and CYP1A1 and susceptibility to cirrhosis or
pancreatitis in alcoholics. Mutagenesis 2004; 19(4):
291–298.
30. Domanski JJ, Nelson LA, Guthrie FE, Domanski RE,
Mark R, Postlethwait RW. Relation between smoking
and levels of DDT and dieldrin in human fat. Arch
Environ Health 1977; 32(5): 196–199.
Address for correspondence: Pascale R. Salameh, Jdeidet El Meten,
Chalet Suisse Street, Ramza Azzam bldg, 5th floor, Beirut, Lebanon
Phone: +961-3-385542; Fax: +961-9-934164;
E-mail: pascalesalameh@yahoo.com.