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The current study aimed to assess the effect of the concomitant exposure to noise and pesticides on the auditory and vestibular systems of endemic disease combat agents. The sample comprised 58 participants, males, divided into two groups. The exposed group (EG) comprised 40 agents, adults, exposed to the noise and pesticides. The control group (CG) comprised 18 participants, without exposure, paired according to age range and gender. The participants from both groups underwent conventional pure-tone audiometry and high-frequency audiometry, evoked otoacoustic emissions and suppression of the emissions, immittance testing, brainstem evoked response audiometry, and dichotic digits test. The vestibular assessment was only carried out in the experimental group. Results showed no difference between the groups in the findings of the pure-tone audiometry and suppression effect of the evoked otoacoustic emissions. Difference was evidenced between the groups in the acoustic reflex testing, the tympanometry, the brainstem evoked response audiometry, and the dichotic digits test, with worse results among the EG. In the vestibular assessment, there was the prevalence of altered tests among EG in 36.4% of the cases, more evidence for the peripheral vestibular dysfunction. In conclusion, noise and pesticide exposure impaired the auditory and vestibular systems of endemic disease control agents.
*Address all correspondence to: adriana.lacerda@umontreal.com
1. Introduction
Organophosphate pesticides can change the efferent auditory system’s mechanism of action. Such a change is caused by the inhibition of acetylcholinesterase, which in turn leads to an accumulation of acetylcholine in the peripheral and central auditory pathways [1, 2, 3, 4], affecting the action potential of the efferent system from the superior olivary nucleus to the cochlea [3, 5, 6]. This way, in humans the exposure to pesticides including organophosphate and/or pyrethroid, either alone or in combination with noise, damages the peripheral auditory system [7, 8, 9, 10] and the central auditory functions [3, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22] as well as vestibular function [8, 10, 21].
There is evidence that hearing loss can be considered an early manifestation of chronic intoxication by pesticide [23]. For this reason, both basic and complementary audiological assessments contribute to early identifying the intoxication and determine the causal nexus in the pesticide-exposed populations [6, 24, 25].
Endemic disease combat agents (EDCA) are not only the most exposed healthcare professionals to pesticides [26] but also to the noise from the motorized knapsack sprayers and vehicle-mounted ultra-low volume (ULV) aerosol generators. Even though noise levels have been reported in few studies on pesticide exposure, their assessment is recommended [1, 2, 3, 4, 5, 6, 27].
The EDCA, Public Health professionals who prevent and fight environmental diseases, like dengue, Chagas, Leishmaniosis, and malaria [28]. Their job entails surveillance of houses, waste land, warehouses, and commercial facilities. In addition, they guide the population in the prevention and treatment of infectious diseases, and they manipulate (liquid preparation) and apply larvicides and insecticides to fight vectors [29]. The contamination may occur by skin absorption and inhalation, mainly among agents who make use of the mist-spraying system [30].
Thus, the current study aimed to assess the effect of the concomitant exposure to noise and pesticides on the hearing system and vestibular system of endemic disease combat agents.
It is a cross-sectional, field study, quantitative and descripture, approved by the Research Ethics Committee (REC) of the Worker's Hospital/SES/PR by Plataforma Brasil, protocol number 1.242.014. Please be informed that all ethical precepts have been respected, including the Informed Consent Forms (ICF).
It was developed at the speech-language-hearing university clinic of a private university, with civil servants of the state of Paraná, Brazil. It partnered with the Syndicate of Federal Civil Servants in Health, Labor, Social Security, and Welfare of the State of Paraná (SindPrevs/PR), Federal University of Paraná, Paraná State Department of Health, and the Public Ministry of Labor.
The inclusion criteria for the exposed group encompassed being an endemic disease control agent, being a civil servant of the State of Paraná, and being over 18 years old. The exclusion criterion was having conductive hearing loss. Recruitment was an oral invitation by the person responsible for the SindPrevs/PR; to those who were interested, the union offered transportation to the site of the field study.
The inclusion criterion for the control group was being of the same age group and gender as the exposed group. The exclusion criteria encompassed not having an occupational history of exposure to physical and chemical agents and the presence of conductive and/or mixed hearing loss. Recruitment was an invitation letter from the researchers.
The study sample comprised 58 professionals, divided into two groups. The Exposed Group (EG) entailing 40 EDCA, all males, ages ranging from 48 to 72 years, occupationally exposed to noise and pesticides such as organophosphates and pyrethroids insecticides (as well as a history of past exposure to other types of pesticides, such as organochlorines, carbamates, and larvicides), generated by automatic pesticide sprayers on average for 31.33 years (range of exposure from 20 to 42 years. Tasks performed by the EDCA included pesticide preparation, application, and material cleaning after application. Pesticides were applied by spraying the poison via backpack pump, hand pump, and tracked vehicles.
Usually, the EDCA is exposed to noise and pesticides for 6–10 h a day on average, besides the time they take maintaining the equipment preparing the substances. For example, the exposure time of the backpack Ultra Low Volume (ULV) can be up to eight hours a day, avoiding the hours of intense sunlight.
According to information provided by the Union of Federal Health, Labor, Social Security, and Social Project Civil Servants, Parana State/Brazil, noise levels generated by motorized knapsack sprayers are 107 dBA/4h (Leq decibel in weighting A for four hours), while the vehicle-coupled heavy ULV generates a 75 dBA/4h noise inside the vehicle with closed windows and 110 dBA/4h outside the vehicle. Regarding the use of personal protective equipment, 27 (82%) EDCA reported using hearing protectors, also wearing a breathing mask, disposable clothing, hats, boots, waterproof gloves, and goggles. The Control Group (CG), comprised of 18 workers, males, aged over 48 years (mean = 56 years old; SD-5.6), from several occupational areas, with no history of exposure to chemical or physical agents.
During the hearing screening, two participants were excluded from the EG featuring mixed hearing loss, thus totaling a sample of 38 endemic disease control agents. No participants were excluded from the CG.
Data collection was performed on a single day, from 7:30 a.m. to 11:00, with groups of three to four workers per day/evaluated. In total, there were six months for data collection, according to the following steps: (1) external acoustic meatus screening, (2) conventional pure-tone audiometry and high-frequency audiometry, (3) immittance testing, (4) transient evoked and distortion-product otoacoustic emissions (TEOAE, and DPOAE), (5) suppression effect otoacoustic emissions, (6) brainstem evoked response audiometry (BERA), (7) dichotic digits test (DDT) in the step integrating bilateral and (8) the vestibular function evaluation is composed of many labyrinthine function and ocular tests. The first part of the evaluation was clinical and consisted of Brandt & Daroff’s maneuver.
Data collection was carried out using descriptive statistics. Non-parametric tests were used to compare results between the groups (EG and CG). The results of the study’s groups were compared through the t-test, Fisher’s exact, chi-square, and Pearson correlation, according to each appropriate situation, with a significance level of 0.05 (5%).
In the conventional audiometry, at frequencies between 250 Hz and 8000 Hz, there was no difference in the means of the tone thresholds between the groups, and there was no difference between the EG and CG in the means of the tone thresholds at high frequencies (9000–16,000 Hz), once p-value, measured by means of the Mann-Whitney statistical test, was greater than 0.05 (5%) for each analyzed frequency.
By verifying the occurrence of hearing loss in the conventional audiometry, in the EG, 15 (39.5%) right ears and 13 (34.2%) left ears were considered normal at all frequencies, while neurosensory hearing loss was evidenced in 23 (60.5%) right ears and 25 (65.8%) left ears. In the CG, 9 (50%) right ears and 9 (50%) left ears were considered normal at all frequencies, while neurosensory hearing loss was evidenced in 9 (50%) right ears and 9 (50%) left ears. Binaurally, greater occurrence of hearing loss in the EG than in the CG was observed. However, such differences were not considered significant by applying the Chi-Square Test (RE = p-value 0.46, and LE-p-value 0.26).
In the tympanometric findings for the EG, 31 right ears and 33 left ears were considered normal, that is, no alteration in the tympanus-bone system, while in the CG, 16 right and left ears were considered normal. Tympanometric alterations were AD, AS, and C-type curves. By comparing the findings in the tympanometry, G-Test showed differences between the EG and CG in the right ear (p = 0.0374), that is, there was greater number of tympanometric anomalies in the EG than in the CG. Between the groups, that difference was not evidenced in the left ear (p = 0.8232).
Regarding the acoustic reflex (stapedius) testing, ipsilateral and contralateral pathways, greater number of reflex absences in the EG was observed, as shown in Table 1.
Hertz
RE (afference)
P
LE (afference)
P
Present
Absent
Present
Absent
500 C
EG
32
5
0.3508
29
7
0.1735
CG
17
1
17
1
1000 C
EG
30
7
0.1839
26
10
0.1486
CG
17
1
16
2
2000 C
EG
26
11
0.1156
25
11
0.0352*
CG
16
2
17
1
4000 C
EG
22
15
0.0246*
20
16
0.0962
CG
16
2
14
4
500 I
EG
30
6
0.0754
32
5
0.1253
CG
18
0
18
0
1000 I
EG
29
7
0.0471*
30
7
0.0507
CG
18
0
18
0
2000 I
EG
30
6
0.0754
32
5
0.1253
CG
18
0
18
0
4000 I
EG
27
9
0.0177*
26
11
0.1156
CG
18
0
16
2
Table 1.
Occurrence of presence/absence of the acoustic reflex, contralateral and ipsilateral pathways, among the participants of the exposed group (EG) and control group (CG), separated by right and left ears.
Legend: C = contralateral; I = ipsilateral; RE = right ear; LE = left ear.
Fisher’s Exact Test at the level of significance of 0,05 (significant p-value*).
By comparing the present/absent results of the acoustic reflex, by means of the Fisher’s Exact Test, difference between the groups was observed in the right ear at 1000 Hz and 4000 Hz, ipsilateral pathway, and at 4000 Hz, contralateral pathway. In the left ear, that difference was observed at 2000 Hz, contralateral pathway.
By taking into consideration the normality of the tympanus-bone system, and the normality of the tone hearing thresholds between the frequencies of 500 Hz and 4000 Hz, the TEOAE testing was held. In the EG, passing rates were 88.89% in the right ear, and 82.35% in the left ear, while in the CG, passing rates evidenced 92.31% in the right ear and 93.33% in the left ear. Despite greater passing rates in the CG in the TEOAE, when comparing the findings between the groups, there was no statistical difference, by means of the Fisher’s Exact Test, p-value for the right ear = 0.64 and p-value for the left ear = 0.35. Similar finding was verified in the DPOAE testing, no statistical difference, by means of the Wilcoxon Test, between the groups, in the signal/noise relation at frequency bands of 1501, 2002, 3003, 4004, 6006, and general response (p ≥ 0.05).
In the suppression effect of the TEOAE testing, greater occurrence of the suppression effect was verified in the participants of the CG than in the EG (Figure 1), expressed in percentages. However, by comparing the results of the suppression effect, present and absent, between the groups (EG and CG), by means of the Fisher’s Exact Test (RE), and the Chi-Square Test (LE), no difference was evidenced between the groups, in the right ear (p = 0.2478), as well as in the left ear (p = 0.5466).
Figure 1.
Percentage of occurrence of the suppression effect in the TOAE testing among the participants, right ears (RE) and left ears (LE). Legend: RE = right ear; LE = left ear; EG = exposed group; CG = control group.
Regarding the findings of the brainstem evoked response audiometry (BERA), the statistical difference can be observed, using the student’s t-test, between the groups (EG and CG) in the absolute latencies of waves III (right and left ears), and V (right ear), as well as in the latency interpeak I-III (right and left ears), and I-V (right ear) (Table 2).
BERA
Mean
SD
P
Wave I
RE
EG (N = 32)
1.65
0.12
0.1686
CG (N = 18)
1.62
0.07
LE
EG (N = 31)
1.64
0.12
0.1018
CG (N = 18)
1.60
0.07
Wave III
RE
EG (N = 32)
3.88
0.19
0.0090*
CG (N = 18)
3.76
0.11
LE
EG (N = 31)
3.91
0.18
0.0013*
CG (N = 18)
3.76
0.12
Wave V
RE
EG (N = 32)
5.82
0.30
0.0185*
CG (N = 18)
5.66
0.13
LE
EG (N = 31)
5.82
0.27
0.0843
CG (N = 18)
5.72
0.18
Interpeak I-III
RE
EG (N = 32)
2.24
0.19
0.0403*
CG (N = 18)
2.15
0.13
LE
EG (N = 31)
2.27
0.16
0.0041*
CG (N = 18)
2.15
0.12
Interpeak III-V
RE
EG (N = 32)
1.94
0.19
0.1595
CG (N = 18)
1.89
0.12
LE
EG (N = 31)
1.91
0.20
0.1739
CG (N = 18)
1.96
0.13
Interpeak I-V
RE
EG (N = 32)
4.17
0.30
0.0450*
CG (N = 18)
4.04
0.14
LE
EG (N = 31)
4.18
0.22
0.1328
CG (N = 18)
4.11
0.19
Amplitude I’
RE
EG (N = 32)
0.12
0.09
0.4443
CG (N = 18)
0.09
0.04
LE
EG (N = 31)
0.13
0.06
0.1478
CG (N = 18)
0.11
0.07
AmplitudeV’
RE
EG (N = 32)
0.25
0.12
0.5000
CG (N = 18)
0.25
0.10
LE
EG (N = 31)
0.27
0.11
0.1206
CG (N = 18)
0.23
0.12
Table 2.
Mean and standard deviation of the absolute latencies, interlatencies, and amplitudes of waves I and V, right and left ears of the exposed (EG) and control (CG) groups.
Student´s t-test at the level of significance of 0.05 (significant p-value*).
Legend: RE = right ear; LE = left ear; EG = exposed group; CG = control group; SD = standard deviation.
In relation to the scores of the Dichotic Digits Test (DDT)—binaural integration stage, only participants with mean hearing thresholds up to 25 dB HL at frequencies from 500 to 4000 Hz were included in the DDT analyses. Hence, the exposed group comprised 30 participants, and the control group, 14 participants. The boxplot (mean, standard deviation, minimum, and maximum) for the right ear, left ear, and binaural DDT results are shown in Figure 2. There is a great variation in DDT results among those exposed, which did not happen in the nonexposed group.
Figure 2.
Boxplot of the exposed group’s (EG) and control group’s (CG) participants’ score in the Dichotic Digits Test (DDT) of the right ear (RE), left ear (LE), and binaural (BI).
Regarding the findings of the vestibular assessment, only carried out with the participants of the EG, 63.7% of the 33 EDCA featured vestibular testing within normal standards, 36.3% of them had alterations in the exams, of which 15.2% presented with right deficit peripheral vestibular dysfunction (n = 5), 12.1% with left deficit peripheral vestibular dysfunction (n = 4), and 9% presented irritative peripheral vestibular dysfunction (Figure 3). The prevalence rate of altered results was the 12/33 (p = 0.364).
Figure 3.
Vestibular examination result (N=33). Legend: NVE = normal vestibular exam; RPDVD = right deficit peripheral vestibular dysfunction; LPDVD = left deficit peripheral vestibular dysfunction; IPVD = irritative peripheral vestibular dysfunction; RIPVD = right irritative peripheral vestibular dysfunction; LIPVD = left irritative peripheral vestibular dysfunction.
By Fisher’s Exact Test, there was no significant statistical correlation between age range (p = 0.1132) and time of exposure to risk agents (p = 0.2825). However, by means of the Mann-Whitney non-parametric test, the participants who evidenced worse auditory thresholds in the right ear at the frequency of 4000 Hz (p = 0.0494), also featured abnormal results in the vestibular assessment.
The results in the current study suggest that the simultaneous exposure to noise and pesticides (used in the Public Health) possibly affected some areas of the peripheral and central auditory system, as well as of the peripheral vestibular system in endemic disease control agents.
However, the impact of that exposure on conventional and high-frequency auditory thresholds on the cochlear physiology, on the efferent medial auditory system, and on the central vestibular system, was not confirmed in the current study, probably due to the size and/or age range of the sample. To confirm the effects on those areas, the use of a similar protocol would be interesting in further studies, with a larger and younger sampling, being held in the country or abroad.
The results of the effects of pesticides associated to noise in the peripheral auditory system showed that there was no difference in the means of the auditory thresholds in the conventional and high-frequency audiometry between the studied groups. Similar results were evidenced in another study [19].
Regarding the tympanometric findings, in the EG, greater number of tympanometric abnormalities were observed in the right ear than in the CG, thus, pesticides may affect the middle ear cavity. Even though this result is observed in other studies with pesticide-exposed populations [31, 32], that finding should be further investigated.
Concerning the findings of the acoustic reflex, EG participants evidenced greater number of absent cases than the CG. Similar findings were observed in other studies with populations exposed to otoagressive agents [19, 31, 32, 33]. It can be inferred that, despite the presence of neurosensory hearing loss, there were worse results in the acoustic reflex among the population exposed to pesticides and noise, and the exposure to such harmful agents may lead to damages in the afferent hearing pathways.
In relation to the findings of the evoked otoacoustic emissions, there was no statistical difference regarding signal/noise in the transient stimuli, as well as in the product of distortion. However, it was possible to observe greater levels of responses in the group of participants not exposed to pesticides and noise. Similar observation was verified in the pass/fail of the TEOAE. That finding can be justified by the age factor of the studied population (EG and CG), as all organs undergo organic changes along the years [34].
Regarding the effects of the pesticides associated to noise in the central nervous system, assessed by means of the brainstem evoked response audiometry (BERA), dichotic digits testing (DDT) and suppression effect of the otoacoustic emissions, results evidenced greater impact of pesticides associated to noise on the BERA and DDT, with worse results for the group of participants exposed to pesticides and noise than in the control group. These findings evidence the fact that the central hearing functions of the exposed population have been impaired using pesticides associated to noise.
When assessing the central auditory system of endemic disease combat agents who are exposed to pyrethroid and organophosphate insecticides, the authors identified 56% of central auditory dysfunction, whose relative risk was 7.58. Similar results were observed in other studies with farmworkers exposed to organophosphate pesticides [14] and herbicides, insecticides, and fungicides [17]. Through the long-latency potential (P300), authors verified an increase in the latency of farmworkers exposed to organophosphate insecticides [13]. Such a result suggests that chronic exposure to the pesticide can delay the neurophysiological processes and alter the central auditory system. The same results were observed in a study involving 14 workers responsible for spraying organophosphate insecticides [20].
However, in the suppression effect testing, no difference was observed between the studied groups, which can be attributed to the age range of the sampling in the current study, as age increases, mainly from 60 years and over, there is significant reduction in the suppression effect of the otoacoustic emissions, fundamentally when ipsilateral and contralateral effects are assessed [35].
Concerning the findings of the vestibular screening, 1/3 of the endemic disease control agents were observed to feature peripheral vestibular abnormalities, related to the anterior and posterior labyrinth, once there was statistical difference between the tonal auditory thresholds, at the frequency of 4000 Hz in the right ear, and the abnormal results of the vestibular screening. This finding may be consistent with Cochlear-Vestibular Syndrome. This known fact in the literature justifies the importance of researching the system's integrity through the auditory exams and the vestibular exams [36]. In a study, hearing normality was verified by conventional audiological evaluation, among 61.14% of 18 rural workers exposed to organophosphate insecticides. While 16 workers had irritative peripheral body balance disorder and seven workers had sensorineural hearing loss, thus suggesting that agricultural pesticides cause vestibular alterations through a slow and silent intoxication [37].
The results presented lead to the conclusion that exposure to pesticides and noise (used in Public Health) possibly affected some areas of the peripheral and central auditory system, as well as of the peripheral vestibular system in endemic disease control agents. And induces harmful effects on the central auditory functions, particularly on the brainstem and figure-ground speech-sound auditory skill, identified through the brainstem auditory evoked potentials and the dichotic digits test. The most common peripheral vestibular effect was of the deficit type, revealing the chronicity of the condition.
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Written By
Adriana Bender Moreira de Lacerda, Patrícia Arruda de Souza Alcarás, Maria Cristina Alves Corazza, Adrian Fuente and Bianca Simone Zeigelboim
Submitted: 25 March 2022Reviewed: 06 May 2022Published: 03 June 2022
Open access peer-reviewed chapter
