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Respiratory Health of Plywood Workers Occupationally Exposed to Formaldehyde a
Tan Malaka M.D., Dr. P.H. & Arthur M. Kodama Ph.D.
a
a
School of Public Health University of Hawaii , Honolulu, Hawaii, USA Published online: 03 Aug 2010.
To cite this article: Tan Malaka M.D., Dr. P.H. & Arthur M. Kodama Ph.D. (1990) Respiratory Health of Plywood Workers Occupationally Exposed to Formaldehyde, Archives of Environmental Health: An International Journal, 45:5, 288-294, DOI: 10.1080/00039896.1990.10118748 To link to this article: http://dx.doi.org/10.1080/00039896.1990.10118748
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Respiratory Health of Plywood Workers
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Occupationally Exposed to Formaldehyde
TAN MALAKA, M.D., Dr. P.H.* ARTHUR M. KODAMA, Ph.D. School of Public Health University of Hawaii Honolulu, Hawaii
ABSTRACT. This study was undertaken to enlarge our understanding of the adverse health effects of formaldehyde exposure in the workplace and community environment. The respiratory health status of 186 male plywood workers was evaluated by spirometric tests, respiratory questionnaires, and chest x-rays. Area concentrations of formaldehyde were measured in the work environment and found to range from 0.28 to 3.48 ppm. The average personal exposure was to 1.1 3 ppm of formaldehyde. Exposure to formaldehyde was associated with decrements in the baseline spirometric values, i.e., forced expiratory volume in 1 sec (FEV, ", forced expiratory volume/forced vital capacity (FEV/FVC), and FEF,,,-,,,, and with several respiratory symptoms and diseases, including cough, phlegm, asthma, chronic bronchitis, and chest colds. The results of the study support the hypothesis that chronic exposure to formaldehyde induces symptoms and signs of chronic obstructive lung disease.
FORMALDEHYDE i s a chemical of metabolic, medical, industrial, and societal importance. It is used widely in the chemical, construction, textile, paper, plastic, paint, adhesive, and cosmetic industries. I t s incorporation into the resin of construction material, such as plywood and particle board, and i t s subsequent out-gassing has created a source of formaldehyde exposure in the nonoccupational environment. Because this chemical is ubiquitous, a thorough understanding of its potential health effects is important. Several published reports of case studies and industrial experiences suggest that exposure to formaldehyde is associated with adverse effects on respiratory In addition, the specter of carcinogenicity i n humans has been raised by the demonstration of nasal cancer i n formaldehyde-exposed rats.5 The results of epidemiological studies investigating chronic effects of formaldehyde exposure on pulmonary function, however, are still controversial. 288
Some i n v e ~ t i g a t o r s , ' , ~found , ~ . ~ that after a few years of exposure to formaldehyde, workers experienced a decrease in pulmonary function. Other invest i g a t o r ~ ' ,found ~ that chronic exposure to the chemical was not associated with pulmonary function deficits. Recent studies of controlled human exposure in experimental chambers have also been inconclusive. 9-1 ' The present study sought to evaluate the respiratory health of plywood workers who are chronically exposed to formaldehyde vapor on the job. The objectives were to evaluate the effect of formaldehyde on (1) chronic obstructive airway diseases, (2) acute transitory pulmonary function deficits, and (3) the frequency of respiratory symptoms and diseases. ~~
*Dr. Malaka's current address is: PPLH-UNSRI, Palembang, Indonesia.
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Materials and Methods
The study was conducted at the PT.NS Plywood Company in Gresik, East Java, Indonesia. A matching procedure was used in the design of the study. The population of exposed workers was identified by measurements of environmental formaldehyde at various locations within the plant complex. A random sample of 100 workers, stratified by smoking habit and length of service (< 5 y and 2 5 y), was selected to represent the exposed group. Another 100 workers, matched for age, ethnicity, and smoking habit, were selected from a nonexposed population, i.e., workers with no previous or current exposure to formaldehyde based on occupational histories and the environmental measurements (referent group). Ninety-three exposed subjects and 93 from the referent group completed the baseline pulmonary function tests and interviews. Fifty-five exposed subjects and 50 referent subjects participated in the across-shift spirometric measurements. A total of 20 subjects-I0 selected randomly from each group-were examined by chest roentgenography. Occupational exposures to formaldehyde and dust were measured as area concentrations and personal exposures. In addition, 10 homes of workers were similarly monitored to consider potential exposures to formaldehyde and dust outside the workplace. A STC Professional Formaldehyde Monitoring Kit, developed by Air Technology Lab, Inc., was used for the sampling and analysis of environmental formaldehyde. The STC passive dosimeter system consists of a “passive bubbler” sampler and a compact dedicted colorimeter.12 The colorimetric method used in the STC Formaldehyde Kit is the 3-methyl-2benzot hiazoline hyd razone hydrochloride (MBTH) method recommended by the American Public Health A~sociation.‘~ Dust concentrations were determined gravimetrically using PVC filters and personal air sampling pumps. For total dust determinations, the filters were used in an “open-face” mode, and for respirable dust, miniature cyclones were used as pre-separators. Baseline and across-shift spirometric measurements were conducted to assess the respiratory health of the study subjects. Baseline measurements were carried out upon return to work after a vacation or on a Monday of a regular work schedule. The across-shift measurement was taken % h before the end of a workshift. A Puritan-Bennet VS 400 Spirometer, which complies with American Thoracic Society (ATS) and National Institute for Occupational Safety and Health/Occupational Safety and Health Administration (NIOSH/OSHA) specifications, was used in the study.14 Spirometric procedures recommended by the ATSq5were followed. For analysis of spirometric results, the predicted values for forced expiratory volume in 1 sec (FEV, ),, and forced vital capacity (FVC) were calculated using the formula developed by DaCosta and Coh.Ih For FEF259/o.759/o, the predicted value was calculated using the formula developed by Crapo et a1.I7with an 85% correction facSepternbedOctober1990 [Vol. 45 (No. 5)]
tor suggested by Horvath.l8 For the determination of whether derived values were within normal limits, the residual and ATS methodslqwere used. A standardized respiratory questionnaire, ATSDLD-78-A,Lowas used to detect respiratory symptoms and diseases among study subjects. Modifications were made to the occupational history questions so that past exposures to formaldehyde and dust could be estimated. A sub-sample of 10 subjects selected randomly from each of the exposed and referent groups was examined by chest x-ray at a nearby hospital in Gresik. The results were interpreted by a radiologist at the hospital, and the reports were sent to the investigators. Relationships between the study variables and lung function values were analyzed using simple correlation techniques. Stepwise multiple regression was used to analyze the relationships between lung function and the study variables. When comparing the effect of formaldehyde on lung function of the exposed and referent groups, analysis of covariance (ANCOVA) was used. The association between exposure to formaldehyde and respiratory symptoms and diseases was analyzed by multiple logistic regression. Results Characteristics of the study subjects. A total of 186 Malay male employees of the plywood company were able to complete the study protocol. The participation rate, therefore, was 93%. Table 1 shows the characteristics of the study subjects by group. The small differences in age, height, and weight between the exposed and referent groups were not significant. In terms of pack-years, smokers in the referent group smoked slightly more than those in the exposed group, but the difference was not statistically significant. The small difference in average length of service was statistically significant, with the referent group having worked slightly longer than the exposed group. Environmental formaldehyde. The area concentrations of formaldehyde in the different working units are given in Table 2. The highest concentrations were found in the particle board unit, with a range of 1.16 to 3.48 ppm and an average concentration of 2.36 ppm. Important concentrations were also recorded in the plywood and block board units. Subjects selected for the exposed group worked in these units. Formaldehyde concentrations in the logistic warehouse, sawmill, log pond, and woodworking units, where formaldehyde was not used, ranged from 0.003 to 0.07 ppm and were considered “background” levels. Subjects of the referent group came from the latter locations. Three indicators were developed to estimate the formaldehyde exposure level of the exposed study subjects: (I) AREAFORM, (2) COMFORM, and (3) 289
Table 1.-Demographic
Data of Study Subjects by Group
Exposed ( n = 93)
Age ( y ) Height (cm) Weight (kg) Smoking: Smokers Nonsmokers Pack-years* Length of Service (y)
Referent (n = 93)
Mean
SD
Mean
5D
26.6 163.1
3.6 5.5 6.5
28.8 163.8 52.4 53 40 4.1 6.7
3.9 4.6 5.5
NS NS NS
5.0 2.3
NS
50 9 53
40 3.7 6.2
4.5 2.4
S
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Notes: S = significant; NS = not significant. *Pack-years i s the product of the number of packsid smoked multiplied by the number of years.
CURFORM. AREAFORM is an estimate of cumulative formaldehyde exposure calculated from area concentrations and length of service in the current job. COMFORM is calculated as the personal exposure multiplied by the length of service in the current job, plus the area concentrations times the length of service in previous jobs. CURFORM is the current personal level of exposure. In a preliminary analysis of the data, it was found that AREAFORM provided the largest "variance explained," or R z , and more consistent values. Consequently, AREAFORM was used in the further statistical analysis presented in this paper. The average value of AREAFORM in the exposed group was 6.29 ppm-y with a standard deviation of 2.72. Environmental dust. The results of the dust measurements are presented in Table 3 . The highest concentrations of total and respirable dust were found in the particle board unit. For analysis, cumulative exposure levels for dust were developed using the area concentrations of dust and the length of service of individual workers in their units. For total dust (TDUST) exposures, the difference between the exposed and referent groups was not significant. For respirable dust (RDUST) exposures, there was a statistically significant difference with an average of 2.88 mg/m-l-y for the exposed group and 3.98 mg/m3y for the referent group.
Table 4.-Means
Table 2.-Formaldehyde
Unit
Block board Logistic warehouse' Sawmill' Log pond* Woodworking*
,
~~
Range
Mean
n
0.384.61
0.50 0.07 0.02 0.07 0.003
6 1 1 1
-
-
1
~~
*Formaldehyde not used
,
I
Table 3.-Dust
Concentrations by Unit (mghn')
1
I
Unit
Respirable dust
Total dust
0.47 1.30 0.62 0.73 0.17 0.60
0.77 5.78 1.28 2.16 0.28 1.35
Plywood Particle board Block board Sawmill Logistic warehouse Average
of Baseline Spirometric Values (Adjusted for Dust) by Group
Exposed
Referent
Criteria
Mean
SD
FEV, (1) FVC (I) FEF,.-,I
2.78 3.28 3.04
0.41 0.44 0.76
(11s)
Concentrations by Unit (pprn)
Mean
2.82 3.37 3.44
SD
P'
0.30 0.36 0.78
.001
,272
.ooo
'ANCOVA with dust as a covariate. 1
290
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i
based on the residual method. The ATS method" was employed for FEV, JFVC to predict the presence or absence of an obstructive airway condition. The prevalence of an obstructive airway condition among the subjects exposed to formaldehyde was 3.2%. To determine whether a dose-response relationship could be established for decrements i n pulmonary function, the exposed subjects were classified according to the exposure level based on AREAFORM estimates. Those with an exposure level of 5 ppm-y or more were grouped as "high," and those with less than 5 ppm-y were grouped as "low." The referent group was considered to have no exposure. The results are given i n Table 6 as percentages of predicted spirometric values. Table 7 shows the multiple regression coefficients for age, height, weight, cigarettedd, dust, and formaldehyde as dependent variables. Age was negatively associated with FEV, FEV/FVC, and FEF2506-7501n. Daily cigarette consumption was negatively associated with FEV, ,$FVC and FE.,F.,, Dust as TDUST or RDUST was not a good predictor for any of the spirornetric criteria used in the study. Formaldehyde, given as AREAFORM, was a significant predictor for FEV, o, FEV, dFVC, and FEF25vo-,50A. Table 8 shows the results of the across-shift spirometric measurements. I n both the exposed and re-
Spirometry. Baseline spirometric values of the study subjects (Table 4) are reported as means for the exposed and referent groups after adjusting for the exposure indicator, RDUST, using the Analysis of Covariance (ANCOVA). The exposed group had significantly lower values for FEV,,,, FEV,,,jFVC, and FEF25yo-,5yo. The FVC was not significantly different between the two groups. The prevalence of spirometric abnormalities among the study subjects i s presented in Table 5. For FEV FVC, and FEV,,-,5yo, the determination was
,,",
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Table 5.-Prevalence of Spirometric Abnormalities* among Study Subjects
Exposed
Referent
Criteria FEV, (1) FVC (1) FEV, JFVC ( % ) FEF,,, 7rx tl/s)
16 15 3 11
19 4 16 1 32 11 6
6 12 0 3
64 12 9 0 32
1
'FEV,,, FVC, and FEF,,, %,, based o n the Residual M e t h o d FEV, JFVC based on American Thoracic Society Criteria
1
I
Table 6.-Spirometric Values (% of Predicted) by Exposures Classified as None, low, and High Based on AREAFORM Values of 0, < 5, and 2 5, Respectively
i
Criteria AREAFORM (ppm-y) FEV, il FEV, JFVC (%) FVC ( % ) FEF,,., (yo)
Table 7.-Regression
None
Low
In = 93)
(n = 37)
Mean
SD
Mean
SD
Mean
SD
20.0 4.9 9.2 20.0
3.53 87.4 85.3 87.1 79.5
1.06 10.2 6.4 8.4 18.2
8.12 90.8 84.4 91.7 80.0
1.77 12.7 6.5 10.4 20.1
94.4 86.9 92.0 90.4
Equation Coefficients to Predict Pulmonary Function
Independent
Dependent variables
variables
FEV, 0
FVC
Age Height Weight Cigarettesld
-0.015 0.026
- 0.033
Dust
Formaldehyde'
High ( n = 56)
NS NS NS
-0.015
NS - 0.011
NS NS NS
FEV, JFVC -0.241 NS -0.156 - 0.345 NS - 0.347
FEF,,%.7,% - 0.035
NS NS - 0.026 NS - 0.043
Note: NS = not significant. *AREAFORM entered as a continuous variable.
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ferent groups, the pre- and post-shift spirometric values were not significantly different. Prevalence of respiratory symptoms and diseases in the study subjects is shown in Table 9. The multiple logistic regression technique was used to test the ability of GROUP, exposed and referent, to predict the respiratory symptoms and diseases while adjusting for age, smoking status, and dust. The probabilities (Z values) and estimated odds ratio (EOR) are reported. An additional aggregate variable, SCORE, was obtained as the sum of positive responses in the respiratory symptoms and diseases part of the questionnaire. The range of values tor SCORE was from 0 to 22. The average score of respiratory symptoms and diseases among the exposed group was 4.6, whereas that for the referent group was 1.9. This difference was found to be significant by the paired t test. When the relationship between SCORE and the study variables age, dust, smoking status, and GROUP (exposed and referent) were tested using stepwise multiple regression, only GROUP was sig-
nificantly related to SCORE, i.e., there was a significant relationship between SCORE values and exposure to formaldehyde ( p = .027). Discussion
The area concentrations of tormaldehyde found in the present study ranged from 0.22 to 3.48 ppm. In the plywood unit, the highest concentrations were detected in the glue and hotpress departments, with a maximum concentration of 2.30 pprn. In the particle board unit, the average concentration was 2.36 pprn. The results are similar to those reported by others for formaldehyde concentrations in particle board plants.'',?? The Threshold Limit Value-Time Weighted Average (TLV-TWA) of the American Conference of Governmental Industrial Hygienists (ACGIH) for formaldehyde is 1 ppm, and the substance is categorized as a "suspected human carcinogen."ll Thus, the formaldehyde concentrations found in the particle board unit and some departments of the plywood unit 0fte.n exceeded the ACGlH health standard.
Spirometric Values of Exposed ( n = 55) and Referent ( n = 50)
Table 8.-Acros\-Shift Groups
Post - 5 h iit
Pre-shift Criteria
Mean
SD
Mean
SO
I'
2.88
0.38
3.36
0.41 6.4
2 88 3 37 85 5 118
0 w 0 45 5 8
NS N\ N4
0 75
N5
0 0 5 0
N\ N4 NS N\
85.1 3.79
0.79
3.43 85.4 3.29
'NS
=
L 91
0.30 0.35 4.6
2.83
344 W9 3 2.'
0.7h
32
3; 2 77
not significant by paired t test.
~
1
Table 9.-Respiratory
Symptoms and Diseases by Group
I
Symptom
l
Referent
Lst Imated
(Yn)
odd< ratio
P*
53
32
2 5h
44
18 8 4
143
00 00 01 nI 3b
1
Cough ( ( J Phlegm (1') Epi5odes ot C t4 P Ch ro n ic bronc h It i5 W heez i ng Asthma Occupational asthma 5hortness ot breath Chest colds ( C C ) Otf-work due to C C
1
*Probability derived from Z values given by multiple logi5tic regression\ controlling tor age, smoking status, and dust
~
1
'
292
I
Exposed ( "4 J
16 9
9 30 14
28 23 38
3 Ln 1 01
7
1 LO
8 8 17 16 12
h 31 284 1 98 L 74 4 96
00 0L 04
01
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The overall averages for dust concentrations found in the present study were .1.35 mg/m3for total dust and 0.6 mg/m3 for respirable dust. The highest dust concentrations were found in the particle board unit, i.e., 5.78 mg/m3 for total dust and 1.30 mg/m3 for respirable dust. The ACGlH TLV-TWA for total hardwood dust is 1 mg/m3. Because the raw materials used by the plywood company included several types of hardwood, the dust concentrations in the particle board, sawmill, and block board units were considered to exceed the ACGlH health standard. Two indices were developed to estimate the cumulative exposure to dust for all study subjects, TDUST and RDUST, based on total and respirable dust, respectively. When comparing spirometric values between the exposed and referent groups, RDUST was treated as the covariate instead of TDUST, because it was determined that there was no difference in the TDUST index between the two groups. After controlling for the effect of dust as a covariate, we found that there were significant relationships between exposure to formaldehyde and the baseline spirometric values: FEV,.,, FEV,,dFVC, and FEF,5n,o-7s7,,. The relationship was not significant, however, for FVC. The FEV,.,, FEV,,JFVC, and FEF2so,~-7so,o of the exposed group were lower than that of the referent group. A comparable FVC in the presence of lower FEV,,,, FEV,.dFVC, and FEF,, 5yo values among the exposed subjects indicated the changes were probably obstructive in n a t ~ r e . ' ~2s,The ~ ~ ,most important differences in the prevalence of respiratory symptoms and diseases were found for cough, phlegm, and asthma (Table 9). In this study, asthma was defined as an affirmative answer to the question, "Have you ever had an attack of wheezing that made you feel short of breath?"15Asthmatic symptoms among workers exposed to formaldehyde was reported earlier by Hendrick and Lane3and more recently by Nordman et and Burge et The combination of the above symptoms also suggests obstructive lung disorders. It should be noted, however, that when the ATS criteria for obstructive lung disease19 was applied, only three clear-cut cases were detected among the exposed subjects. It is interesting to note that the chronic effects of formaldehyde on pulmonary function were observed when dust-particularly respirable dustwas also present, as in this study and those of others." 4 . 2 R Gamble et a1.2 discussed "the presence of suitable formaldehyde carriers so that it will be carried deeper into the lung where it has a greater biological effectiveness than when deposited in the upper respiratory tract." These observations are also in accord with the long-established findings of Amdur.2yHowever, i n the present study, dust alone was not found to be associated with the baseline spirometric values. No control group without dust exposure was used i n the present study; therefore, the possibility of an interaction between formaldehyde and dust in developing the symptoms and diseases and effects on lung function cannot be ruled out.
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When the dose-response relationship between impairment in pulmonary function and exposure to formaldehyde was considered, the only consistent decrement in spirometric function and exposure level was found for FEV,,,,FVC (Table 6). The firstorder approximations of the dose-response relationships are the regression line slopes given in Table 7. The R* for the effect of formaldehyde exposure was small for all lung function parameters. Although the differences in lung function were, on average, relatively small, which raises questions about its clinical significance, it is clear that exposure to formaldehyde resulted in statistically highly significant decrements in most of the measures of lung function. It has been reported that statistically significant changes in ventilatory capacity are detectable after 5 or more y of exposure to formaldeh ~ d eThe . ~ average length of service of the subjects in the present study was only 6.5 y. We suggest that it may take longer to complete a picture that i s both statistically significant and clinically meaningful. The across-shift spirometric measurements were intended to detect any acute effects of formaldehyde on pulmonary function. An across-shift difference was not demonstrable in the present study, which is consistent with the findings of many experimental (human) studies.9,26, 30, 31 That significant differences were found in the baseline but not in across-shift spirometric values indicates that the underlying mechanism may be a delayed effect mediated by hypersensitivity reactions. This contention is supported by a recent report by Burge et al.27Hypersensitivity as a possible underlying mechanism for formaldehyde asthma has also been suggested by Gamble.32 In the present study, chest x-ray examinations were intended to detect the presence of pulmonary tuberculosis, inasmuch as the disease, particularly in its later stages, presents signs and symptoms that resemble obstructive disorders. The results of the chest x-rays showed that there was a relatively high prevalence of chronic upper respiratory tract infections i n both the exposed and referent groups. The findings were not unexpected because the study was conducted in a developing country where infectious diseases are widespread. One subject i n the referent group had an active case of pulmonary tuberculosis. Presumably, the finding would only bias the study toward negative results. After controlling for effects of age, smoking status, and dust, the association with formaldehyde exposure was found t o be significant for all the respiratory symptoms, except wheezing. The associations were particularly strong for cough, phlegm, asthma, and time off work resulting from chest colds. Any chest disease leading to at least 1 d taken off by the subjects in the last 2 y was recorded as a "yes" for this question. One of the possible reasons for the high prevalence in the off-work variable i s infectious disease. The higher prevalence i n the exposed group may result from an aggravation by formaldehyde. That cough, phlegm, and asthma were 293
strongly associated with formaldehyde exposure is consistent with the findings of spirometric decrements and that the impairments were probably obstructive in nature. Conclusion
The main finding of the study was the statistically significant association between chronic formaldehyde exposure and decrements in pulmonary function. The pattern of changes in spirometric values are compatible with the increased prevalence of cough, phlegm, and asthma among the exposed subjects, which suggest the presence of obstructive pu Im o na ry disease .
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* * * * * * * * * * Submitted for publication Februarv 22,1989; revised; accepted for publication April 9, 1990. Requests for reprints should be sent to: Dr. Arthur M. Kodama, University of Hawaii, School of Public Health, 1960 East-West Road, Honolulu, HI 96822.
* * * * * * * * * * References
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12 Air Technology Labs, Inc. Instruction manual for STC formaldehyde monitoring kit, Version 1.2. Fresno, CA: Air Technology Labs, Inc., 548 East Mallard Circle, 93710. 13 Katz M. (ed). Tentative method of analysis for formaldehyde content of the atmosphere (MBTH-colorimetric methodapplications to other aldehydes). Method of air sampling and analysis. 2nd. ed. Washington, DC: American Public Health Association, pp. 308-13; 1977. 14 Puritan-Bennet Corporation. VS400 operating manual. Wilmington, MA: Puritan-Bennet Corporation of Massachusetts, Boston Division, 265 Ballardvale Street, 01887. 15 Ferris BG. Recommended standardized procedures for pulmonary function testing. Epidemiology Standardization Project. Am Rev Respir Dis 1978; 118:55-88. 16 DaCosta JL, Goh BK. Prediction nomograms for lung function measurements in adult Chinese. Singapore Med J 1971; 12 :192-97. 17 Crapo RO, Morris AH, Cardner RM. Reference spirometric values using techniques and equipment that meet ATS recommendations. Am Rev Respir Dis 1981 ; 123:659-64. 18 Horvath E . Manual of spirometry in occupational medicine. USDHHS-NIOSH, 1981. 19 Hankinson IL. Pulmonary function testing in the screening of workers: guidelines for instrumentation, performance, and interpretation. J Occup M e d 1986; 28:1081-92. 20. Ferris BC. Recommended respiratory questionnaire for use with adults and children in epidemiologic research. Epidemiology Standardization Project. Am Rev Respir Dis 1978; 118:735. 21 Kauppinen TP, Niemela RI. Occupational exposure to chemical agents in particleboard industry. Scan I Work Environ Health 1985; 11:357-63. 22. Wayne LG, Brian Rj, Ziedman K. Irritant effects of industrial chemicals: formaldehyde, NIOSH Publication No. 77-1.17. 1977; USDHEW, PHS, CDC. 23. American Conference of Governmental Industrial Hygienists (ACGIH). Threshold Limit Values (TLV) for chemical substances in the work environment. Cincinnati, O H : ACGIH, 1987. 24. Brook SM. The evaluation of occupational airway disease in the laboratory and workplace. I Allergy Clin lmmunol 1982; 70 :56-66. 25. Wegman DH. Respiratory disorders. In: Levy BS, Wegman DH, eds. Occupational Health; Boston, MA: Little, Brown and CO., 1983; pp. 267-91. 26. iqordman H, Keskinan H, Tuppurainen M. Formaldehyde asthma-rare or overlooked. J Allergy Clin lmmunol 1985; 75 :91-99. 27. Burge PS, Harries MG, Lam WK, et al. Occupational asthma due to formaldehyde. Thorax 1985; 40:255-60. 28. Cockcroft DW, Hoepner M D , Dolovich j . Occupational asthma caused by cedar urea-formaldehyde particle board. Chest 1982; 82:49-53. 29. Amdur MO. The response of guinea pigs to inhalation of formaldehyde and formic acid alone and with sodium chloride aerosol. Int J Pollut 1960; 3:201-20. 30. Frigas E, lellery WV, Reed CE. Bronchial challenge with formaldehyde gas: Lack of bronchoconstriction in 13 patients suspected of having induced formaldehyde asthma. Mayo Clinic Proc 1984; 59:295-99. 31, Schacter EN, Witek TI, Tosun T, et al. A study of respiratory effects from exposure to 2 ppm formaldehyde in health subjects. Arch Environ Health 1986; 41 :229-39. 32. Gamble IF. Effects of formaldehyde on respriatory system. In: Gibson jE, ed. Formaldehyde toxicity. Washington, DC: Hemisphere Publishing Corporation, 1983; pp. 173-97.
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Respiratory Health of Plywood Workers Occupationally Exposed to Formaldehyde a
Tan Malaka M.D., Dr. P.H. & Arthur M. Kodama Ph.D.
a
a
School of Public Health University of Hawaii , Honolulu, Hawaii, USA Published online: 03 Aug 2010.
To cite this article: Tan Malaka M.D., Dr. P.H. & Arthur M. Kodama Ph.D. (1990) Respiratory Health of Plywood Workers Occupationally Exposed to Formaldehyde, Archives of Environmental Health: An International Journal, 45:5, 288-294, DOI: 10.1080/00039896.1990.10118748 To link to this article: http://dx.doi.org/10.1080/00039896.1990.10118748
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Respiratory Health of Plywood Workers
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Occupationally Exposed to Formaldehyde
TAN MALAKA, M.D., Dr. P.H.* ARTHUR M. KODAMA, Ph.D. School of Public Health University of Hawaii Honolulu, Hawaii
ABSTRACT. This study was undertaken to enlarge our understanding of the adverse health effects of formaldehyde exposure in the workplace and community environment. The respiratory health status of 186 male plywood workers was evaluated by spirometric tests, respiratory questionnaires, and chest x-rays. Area concentrations of formaldehyde were measured in the work environment and found to range from 0.28 to 3.48 ppm. The average personal exposure was to 1.1 3 ppm of formaldehyde. Exposure to formaldehyde was associated with decrements in the baseline spirometric values, i.e., forced expiratory volume in 1 sec (FEV, ", forced expiratory volume/forced vital capacity (FEV/FVC), and FEF,,,-,,,, and with several respiratory symptoms and diseases, including cough, phlegm, asthma, chronic bronchitis, and chest colds. The results of the study support the hypothesis that chronic exposure to formaldehyde induces symptoms and signs of chronic obstructive lung disease.
FORMALDEHYDE i s a chemical of metabolic, medical, industrial, and societal importance. It is used widely in the chemical, construction, textile, paper, plastic, paint, adhesive, and cosmetic industries. I t s incorporation into the resin of construction material, such as plywood and particle board, and i t s subsequent out-gassing has created a source of formaldehyde exposure in the nonoccupational environment. Because this chemical is ubiquitous, a thorough understanding of its potential health effects is important. Several published reports of case studies and industrial experiences suggest that exposure to formaldehyde is associated with adverse effects on respiratory In addition, the specter of carcinogenicity i n humans has been raised by the demonstration of nasal cancer i n formaldehyde-exposed rats.5 The results of epidemiological studies investigating chronic effects of formaldehyde exposure on pulmonary function, however, are still controversial. 288
Some i n v e ~ t i g a t o r s , ' , ~found , ~ . ~ that after a few years of exposure to formaldehyde, workers experienced a decrease in pulmonary function. Other invest i g a t o r ~ ' ,found ~ that chronic exposure to the chemical was not associated with pulmonary function deficits. Recent studies of controlled human exposure in experimental chambers have also been inconclusive. 9-1 ' The present study sought to evaluate the respiratory health of plywood workers who are chronically exposed to formaldehyde vapor on the job. The objectives were to evaluate the effect of formaldehyde on (1) chronic obstructive airway diseases, (2) acute transitory pulmonary function deficits, and (3) the frequency of respiratory symptoms and diseases. ~~
*Dr. Malaka's current address is: PPLH-UNSRI, Palembang, Indonesia.
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Materials and Methods
The study was conducted at the PT.NS Plywood Company in Gresik, East Java, Indonesia. A matching procedure was used in the design of the study. The population of exposed workers was identified by measurements of environmental formaldehyde at various locations within the plant complex. A random sample of 100 workers, stratified by smoking habit and length of service (< 5 y and 2 5 y), was selected to represent the exposed group. Another 100 workers, matched for age, ethnicity, and smoking habit, were selected from a nonexposed population, i.e., workers with no previous or current exposure to formaldehyde based on occupational histories and the environmental measurements (referent group). Ninety-three exposed subjects and 93 from the referent group completed the baseline pulmonary function tests and interviews. Fifty-five exposed subjects and 50 referent subjects participated in the across-shift spirometric measurements. A total of 20 subjects-I0 selected randomly from each group-were examined by chest roentgenography. Occupational exposures to formaldehyde and dust were measured as area concentrations and personal exposures. In addition, 10 homes of workers were similarly monitored to consider potential exposures to formaldehyde and dust outside the workplace. A STC Professional Formaldehyde Monitoring Kit, developed by Air Technology Lab, Inc., was used for the sampling and analysis of environmental formaldehyde. The STC passive dosimeter system consists of a “passive bubbler” sampler and a compact dedicted colorimeter.12 The colorimetric method used in the STC Formaldehyde Kit is the 3-methyl-2benzot hiazoline hyd razone hydrochloride (MBTH) method recommended by the American Public Health A~sociation.‘~ Dust concentrations were determined gravimetrically using PVC filters and personal air sampling pumps. For total dust determinations, the filters were used in an “open-face” mode, and for respirable dust, miniature cyclones were used as pre-separators. Baseline and across-shift spirometric measurements were conducted to assess the respiratory health of the study subjects. Baseline measurements were carried out upon return to work after a vacation or on a Monday of a regular work schedule. The across-shift measurement was taken % h before the end of a workshift. A Puritan-Bennet VS 400 Spirometer, which complies with American Thoracic Society (ATS) and National Institute for Occupational Safety and Health/Occupational Safety and Health Administration (NIOSH/OSHA) specifications, was used in the study.14 Spirometric procedures recommended by the ATSq5were followed. For analysis of spirometric results, the predicted values for forced expiratory volume in 1 sec (FEV, ),, and forced vital capacity (FVC) were calculated using the formula developed by DaCosta and Coh.Ih For FEF259/o.759/o, the predicted value was calculated using the formula developed by Crapo et a1.I7with an 85% correction facSepternbedOctober1990 [Vol. 45 (No. 5)]
tor suggested by Horvath.l8 For the determination of whether derived values were within normal limits, the residual and ATS methodslqwere used. A standardized respiratory questionnaire, ATSDLD-78-A,Lowas used to detect respiratory symptoms and diseases among study subjects. Modifications were made to the occupational history questions so that past exposures to formaldehyde and dust could be estimated. A sub-sample of 10 subjects selected randomly from each of the exposed and referent groups was examined by chest x-ray at a nearby hospital in Gresik. The results were interpreted by a radiologist at the hospital, and the reports were sent to the investigators. Relationships between the study variables and lung function values were analyzed using simple correlation techniques. Stepwise multiple regression was used to analyze the relationships between lung function and the study variables. When comparing the effect of formaldehyde on lung function of the exposed and referent groups, analysis of covariance (ANCOVA) was used. The association between exposure to formaldehyde and respiratory symptoms and diseases was analyzed by multiple logistic regression. Results Characteristics of the study subjects. A total of 186 Malay male employees of the plywood company were able to complete the study protocol. The participation rate, therefore, was 93%. Table 1 shows the characteristics of the study subjects by group. The small differences in age, height, and weight between the exposed and referent groups were not significant. In terms of pack-years, smokers in the referent group smoked slightly more than those in the exposed group, but the difference was not statistically significant. The small difference in average length of service was statistically significant, with the referent group having worked slightly longer than the exposed group. Environmental formaldehyde. The area concentrations of formaldehyde in the different working units are given in Table 2. The highest concentrations were found in the particle board unit, with a range of 1.16 to 3.48 ppm and an average concentration of 2.36 ppm. Important concentrations were also recorded in the plywood and block board units. Subjects selected for the exposed group worked in these units. Formaldehyde concentrations in the logistic warehouse, sawmill, log pond, and woodworking units, where formaldehyde was not used, ranged from 0.003 to 0.07 ppm and were considered “background” levels. Subjects of the referent group came from the latter locations. Three indicators were developed to estimate the formaldehyde exposure level of the exposed study subjects: (I) AREAFORM, (2) COMFORM, and (3) 289
Table 1.-Demographic
Data of Study Subjects by Group
Exposed ( n = 93)
Age ( y ) Height (cm) Weight (kg) Smoking: Smokers Nonsmokers Pack-years* Length of Service (y)
Referent (n = 93)
Mean
SD
Mean
5D
26.6 163.1
3.6 5.5 6.5
28.8 163.8 52.4 53 40 4.1 6.7
3.9 4.6 5.5
NS NS NS
5.0 2.3
NS
50 9 53
40 3.7 6.2
4.5 2.4
S
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Notes: S = significant; NS = not significant. *Pack-years i s the product of the number of packsid smoked multiplied by the number of years.
CURFORM. AREAFORM is an estimate of cumulative formaldehyde exposure calculated from area concentrations and length of service in the current job. COMFORM is calculated as the personal exposure multiplied by the length of service in the current job, plus the area concentrations times the length of service in previous jobs. CURFORM is the current personal level of exposure. In a preliminary analysis of the data, it was found that AREAFORM provided the largest "variance explained," or R z , and more consistent values. Consequently, AREAFORM was used in the further statistical analysis presented in this paper. The average value of AREAFORM in the exposed group was 6.29 ppm-y with a standard deviation of 2.72. Environmental dust. The results of the dust measurements are presented in Table 3 . The highest concentrations of total and respirable dust were found in the particle board unit. For analysis, cumulative exposure levels for dust were developed using the area concentrations of dust and the length of service of individual workers in their units. For total dust (TDUST) exposures, the difference between the exposed and referent groups was not significant. For respirable dust (RDUST) exposures, there was a statistically significant difference with an average of 2.88 mg/m-l-y for the exposed group and 3.98 mg/m3y for the referent group.
Table 4.-Means
Table 2.-Formaldehyde
Unit
Block board Logistic warehouse' Sawmill' Log pond* Woodworking*
,
~~
Range
Mean
n
0.384.61
0.50 0.07 0.02 0.07 0.003
6 1 1 1
-
-
1
~~
*Formaldehyde not used
,
I
Table 3.-Dust
Concentrations by Unit (mghn')
1
I
Unit
Respirable dust
Total dust
0.47 1.30 0.62 0.73 0.17 0.60
0.77 5.78 1.28 2.16 0.28 1.35
Plywood Particle board Block board Sawmill Logistic warehouse Average
of Baseline Spirometric Values (Adjusted for Dust) by Group
Exposed
Referent
Criteria
Mean
SD
FEV, (1) FVC (I) FEF,.-,I
2.78 3.28 3.04
0.41 0.44 0.76
(11s)
Concentrations by Unit (pprn)
Mean
2.82 3.37 3.44
SD
P'
0.30 0.36 0.78
.001
,272
.ooo
'ANCOVA with dust as a covariate. 1
290
I
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i
based on the residual method. The ATS method" was employed for FEV, JFVC to predict the presence or absence of an obstructive airway condition. The prevalence of an obstructive airway condition among the subjects exposed to formaldehyde was 3.2%. To determine whether a dose-response relationship could be established for decrements i n pulmonary function, the exposed subjects were classified according to the exposure level based on AREAFORM estimates. Those with an exposure level of 5 ppm-y or more were grouped as "high," and those with less than 5 ppm-y were grouped as "low." The referent group was considered to have no exposure. The results are given i n Table 6 as percentages of predicted spirometric values. Table 7 shows the multiple regression coefficients for age, height, weight, cigarettedd, dust, and formaldehyde as dependent variables. Age was negatively associated with FEV, FEV/FVC, and FEF2506-7501n. Daily cigarette consumption was negatively associated with FEV, ,$FVC and FE.,F.,, Dust as TDUST or RDUST was not a good predictor for any of the spirornetric criteria used in the study. Formaldehyde, given as AREAFORM, was a significant predictor for FEV, o, FEV, dFVC, and FEF25vo-,50A. Table 8 shows the results of the across-shift spirometric measurements. I n both the exposed and re-
Spirometry. Baseline spirometric values of the study subjects (Table 4) are reported as means for the exposed and referent groups after adjusting for the exposure indicator, RDUST, using the Analysis of Covariance (ANCOVA). The exposed group had significantly lower values for FEV,,,, FEV,,,jFVC, and FEF25yo-,5yo. The FVC was not significantly different between the two groups. The prevalence of spirometric abnormalities among the study subjects i s presented in Table 5. For FEV FVC, and FEV,,-,5yo, the determination was
,,",
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Table 5.-Prevalence of Spirometric Abnormalities* among Study Subjects
Exposed
Referent
Criteria FEV, (1) FVC (1) FEV, JFVC ( % ) FEF,,, 7rx tl/s)
16 15 3 11
19 4 16 1 32 11 6
6 12 0 3
64 12 9 0 32
1
'FEV,,, FVC, and FEF,,, %,, based o n the Residual M e t h o d FEV, JFVC based on American Thoracic Society Criteria
1
I
Table 6.-Spirometric Values (% of Predicted) by Exposures Classified as None, low, and High Based on AREAFORM Values of 0, < 5, and 2 5, Respectively
i
Criteria AREAFORM (ppm-y) FEV, il FEV, JFVC (%) FVC ( % ) FEF,,., (yo)
Table 7.-Regression
None
Low
In = 93)
(n = 37)
Mean
SD
Mean
SD
Mean
SD
20.0 4.9 9.2 20.0
3.53 87.4 85.3 87.1 79.5
1.06 10.2 6.4 8.4 18.2
8.12 90.8 84.4 91.7 80.0
1.77 12.7 6.5 10.4 20.1
94.4 86.9 92.0 90.4
Equation Coefficients to Predict Pulmonary Function
Independent
Dependent variables
variables
FEV, 0
FVC
Age Height Weight Cigarettesld
-0.015 0.026
- 0.033
Dust
Formaldehyde'
High ( n = 56)
NS NS NS
-0.015
NS - 0.011
NS NS NS
FEV, JFVC -0.241 NS -0.156 - 0.345 NS - 0.347
FEF,,%.7,% - 0.035
NS NS - 0.026 NS - 0.043
Note: NS = not significant. *AREAFORM entered as a continuous variable.
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ferent groups, the pre- and post-shift spirometric values were not significantly different. Prevalence of respiratory symptoms and diseases in the study subjects is shown in Table 9. The multiple logistic regression technique was used to test the ability of GROUP, exposed and referent, to predict the respiratory symptoms and diseases while adjusting for age, smoking status, and dust. The probabilities (Z values) and estimated odds ratio (EOR) are reported. An additional aggregate variable, SCORE, was obtained as the sum of positive responses in the respiratory symptoms and diseases part of the questionnaire. The range of values tor SCORE was from 0 to 22. The average score of respiratory symptoms and diseases among the exposed group was 4.6, whereas that for the referent group was 1.9. This difference was found to be significant by the paired t test. When the relationship between SCORE and the study variables age, dust, smoking status, and GROUP (exposed and referent) were tested using stepwise multiple regression, only GROUP was sig-
nificantly related to SCORE, i.e., there was a significant relationship between SCORE values and exposure to formaldehyde ( p = .027). Discussion
The area concentrations of tormaldehyde found in the present study ranged from 0.22 to 3.48 ppm. In the plywood unit, the highest concentrations were detected in the glue and hotpress departments, with a maximum concentration of 2.30 pprn. In the particle board unit, the average concentration was 2.36 pprn. The results are similar to those reported by others for formaldehyde concentrations in particle board plants.'',?? The Threshold Limit Value-Time Weighted Average (TLV-TWA) of the American Conference of Governmental Industrial Hygienists (ACGIH) for formaldehyde is 1 ppm, and the substance is categorized as a "suspected human carcinogen."ll Thus, the formaldehyde concentrations found in the particle board unit and some departments of the plywood unit 0fte.n exceeded the ACGlH health standard.
Spirometric Values of Exposed ( n = 55) and Referent ( n = 50)
Table 8.-Acros\-Shift Groups
Post - 5 h iit
Pre-shift Criteria
Mean
SD
Mean
SO
I'
2.88
0.38
3.36
0.41 6.4
2 88 3 37 85 5 118
0 w 0 45 5 8
NS N\ N4
0 75
N5
0 0 5 0
N\ N4 NS N\
85.1 3.79
0.79
3.43 85.4 3.29
'NS
=
L 91
0.30 0.35 4.6
2.83
344 W9 3 2.'
0.7h
32
3; 2 77
not significant by paired t test.
~
1
Table 9.-Respiratory
Symptoms and Diseases by Group
I
Symptom
l
Referent
Lst Imated
(Yn)
odd< ratio
P*
53
32
2 5h
44
18 8 4
143
00 00 01 nI 3b
1
Cough ( ( J Phlegm (1') Epi5odes ot C t4 P Ch ro n ic bronc h It i5 W heez i ng Asthma Occupational asthma 5hortness ot breath Chest colds ( C C ) Otf-work due to C C
1
*Probability derived from Z values given by multiple logi5tic regression\ controlling tor age, smoking status, and dust
~
1
'
292
I
Exposed ( "4 J
16 9
9 30 14
28 23 38
3 Ln 1 01
7
1 LO
8 8 17 16 12
h 31 284 1 98 L 74 4 96
00 0L 04
01
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The overall averages for dust concentrations found in the present study were .1.35 mg/m3for total dust and 0.6 mg/m3 for respirable dust. The highest dust concentrations were found in the particle board unit, i.e., 5.78 mg/m3 for total dust and 1.30 mg/m3 for respirable dust. The ACGlH TLV-TWA for total hardwood dust is 1 mg/m3. Because the raw materials used by the plywood company included several types of hardwood, the dust concentrations in the particle board, sawmill, and block board units were considered to exceed the ACGlH health standard. Two indices were developed to estimate the cumulative exposure to dust for all study subjects, TDUST and RDUST, based on total and respirable dust, respectively. When comparing spirometric values between the exposed and referent groups, RDUST was treated as the covariate instead of TDUST, because it was determined that there was no difference in the TDUST index between the two groups. After controlling for the effect of dust as a covariate, we found that there were significant relationships between exposure to formaldehyde and the baseline spirometric values: FEV,.,, FEV,,dFVC, and FEF,5n,o-7s7,,. The relationship was not significant, however, for FVC. The FEV,.,, FEV,,JFVC, and FEF2so,~-7so,o of the exposed group were lower than that of the referent group. A comparable FVC in the presence of lower FEV,,,, FEV,.dFVC, and FEF,, 5yo values among the exposed subjects indicated the changes were probably obstructive in n a t ~ r e . ' ~2s,The ~ ~ ,most important differences in the prevalence of respiratory symptoms and diseases were found for cough, phlegm, and asthma (Table 9). In this study, asthma was defined as an affirmative answer to the question, "Have you ever had an attack of wheezing that made you feel short of breath?"15Asthmatic symptoms among workers exposed to formaldehyde was reported earlier by Hendrick and Lane3and more recently by Nordman et and Burge et The combination of the above symptoms also suggests obstructive lung disorders. It should be noted, however, that when the ATS criteria for obstructive lung disease19 was applied, only three clear-cut cases were detected among the exposed subjects. It is interesting to note that the chronic effects of formaldehyde on pulmonary function were observed when dust-particularly respirable dustwas also present, as in this study and those of others." 4 . 2 R Gamble et a1.2 discussed "the presence of suitable formaldehyde carriers so that it will be carried deeper into the lung where it has a greater biological effectiveness than when deposited in the upper respiratory tract." These observations are also in accord with the long-established findings of Amdur.2yHowever, i n the present study, dust alone was not found to be associated with the baseline spirometric values. No control group without dust exposure was used i n the present study; therefore, the possibility of an interaction between formaldehyde and dust in developing the symptoms and diseases and effects on lung function cannot be ruled out.
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When the dose-response relationship between impairment in pulmonary function and exposure to formaldehyde was considered, the only consistent decrement in spirometric function and exposure level was found for FEV,,,,FVC (Table 6). The firstorder approximations of the dose-response relationships are the regression line slopes given in Table 7. The R* for the effect of formaldehyde exposure was small for all lung function parameters. Although the differences in lung function were, on average, relatively small, which raises questions about its clinical significance, it is clear that exposure to formaldehyde resulted in statistically highly significant decrements in most of the measures of lung function. It has been reported that statistically significant changes in ventilatory capacity are detectable after 5 or more y of exposure to formaldeh ~ d eThe . ~ average length of service of the subjects in the present study was only 6.5 y. We suggest that it may take longer to complete a picture that i s both statistically significant and clinically meaningful. The across-shift spirometric measurements were intended to detect any acute effects of formaldehyde on pulmonary function. An across-shift difference was not demonstrable in the present study, which is consistent with the findings of many experimental (human) studies.9,26, 30, 31 That significant differences were found in the baseline but not in across-shift spirometric values indicates that the underlying mechanism may be a delayed effect mediated by hypersensitivity reactions. This contention is supported by a recent report by Burge et al.27Hypersensitivity as a possible underlying mechanism for formaldehyde asthma has also been suggested by Gamble.32 In the present study, chest x-ray examinations were intended to detect the presence of pulmonary tuberculosis, inasmuch as the disease, particularly in its later stages, presents signs and symptoms that resemble obstructive disorders. The results of the chest x-rays showed that there was a relatively high prevalence of chronic upper respiratory tract infections i n both the exposed and referent groups. The findings were not unexpected because the study was conducted in a developing country where infectious diseases are widespread. One subject i n the referent group had an active case of pulmonary tuberculosis. Presumably, the finding would only bias the study toward negative results. After controlling for effects of age, smoking status, and dust, the association with formaldehyde exposure was found t o be significant for all the respiratory symptoms, except wheezing. The associations were particularly strong for cough, phlegm, asthma, and time off work resulting from chest colds. Any chest disease leading to at least 1 d taken off by the subjects in the last 2 y was recorded as a "yes" for this question. One of the possible reasons for the high prevalence in the off-work variable i s infectious disease. The higher prevalence i n the exposed group may result from an aggravation by formaldehyde. That cough, phlegm, and asthma were 293
strongly associated with formaldehyde exposure is consistent with the findings of spirometric decrements and that the impairments were probably obstructive in nature. Conclusion
The main finding of the study was the statistically significant association between chronic formaldehyde exposure and decrements in pulmonary function. The pattern of changes in spirometric values are compatible with the increased prevalence of cough, phlegm, and asthma among the exposed subjects, which suggest the presence of obstructive pu Im o na ry disease .
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* * * * * * * * * * Submitted for publication Februarv 22,1989; revised; accepted for publication April 9, 1990. Requests for reprints should be sent to: Dr. Arthur M. Kodama, University of Hawaii, School of Public Health, 1960 East-West Road, Honolulu, HI 96822.
* * * * * * * * * * References
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12 Air Technology Labs, Inc. Instruction manual for STC formaldehyde monitoring kit, Version 1.2. Fresno, CA: Air Technology Labs, Inc., 548 East Mallard Circle, 93710. 13 Katz M. (ed). Tentative method of analysis for formaldehyde content of the atmosphere (MBTH-colorimetric methodapplications to other aldehydes). Method of air sampling and analysis. 2nd. ed. Washington, DC: American Public Health Association, pp. 308-13; 1977. 14 Puritan-Bennet Corporation. VS400 operating manual. Wilmington, MA: Puritan-Bennet Corporation of Massachusetts, Boston Division, 265 Ballardvale Street, 01887. 15 Ferris BG. Recommended standardized procedures for pulmonary function testing. Epidemiology Standardization Project. Am Rev Respir Dis 1978; 118:55-88. 16 DaCosta JL, Goh BK. Prediction nomograms for lung function measurements in adult Chinese. Singapore Med J 1971; 12 :192-97. 17 Crapo RO, Morris AH, Cardner RM. Reference spirometric values using techniques and equipment that meet ATS recommendations. Am Rev Respir Dis 1981 ; 123:659-64. 18 Horvath E . Manual of spirometry in occupational medicine. USDHHS-NIOSH, 1981. 19 Hankinson IL. Pulmonary function testing in the screening of workers: guidelines for instrumentation, performance, and interpretation. J Occup M e d 1986; 28:1081-92. 20. Ferris BC. Recommended respiratory questionnaire for use with adults and children in epidemiologic research. Epidemiology Standardization Project. Am Rev Respir Dis 1978; 118:735. 21 Kauppinen TP, Niemela RI. Occupational exposure to chemical agents in particleboard industry. Scan I Work Environ Health 1985; 11:357-63. 22. Wayne LG, Brian Rj, Ziedman K. Irritant effects of industrial chemicals: formaldehyde, NIOSH Publication No. 77-1.17. 1977; USDHEW, PHS, CDC. 23. American Conference of Governmental Industrial Hygienists (ACGIH). Threshold Limit Values (TLV) for chemical substances in the work environment. Cincinnati, O H : ACGIH, 1987. 24. Brook SM. The evaluation of occupational airway disease in the laboratory and workplace. I Allergy Clin lmmunol 1982; 70 :56-66. 25. Wegman DH. Respiratory disorders. In: Levy BS, Wegman DH, eds. Occupational Health; Boston, MA: Little, Brown and CO., 1983; pp. 267-91. 26. iqordman H, Keskinan H, Tuppurainen M. Formaldehyde asthma-rare or overlooked. J Allergy Clin lmmunol 1985; 75 :91-99. 27. Burge PS, Harries MG, Lam WK, et al. Occupational asthma due to formaldehyde. Thorax 1985; 40:255-60. 28. Cockcroft DW, Hoepner M D , Dolovich j . Occupational asthma caused by cedar urea-formaldehyde particle board. Chest 1982; 82:49-53. 29. Amdur MO. The response of guinea pigs to inhalation of formaldehyde and formic acid alone and with sodium chloride aerosol. Int J Pollut 1960; 3:201-20. 30. Frigas E, lellery WV, Reed CE. Bronchial challenge with formaldehyde gas: Lack of bronchoconstriction in 13 patients suspected of having induced formaldehyde asthma. Mayo Clinic Proc 1984; 59:295-99. 31, Schacter EN, Witek TI, Tosun T, et al. A study of respiratory effects from exposure to 2 ppm formaldehyde in health subjects. Arch Environ Health 1986; 41 :229-39. 32. Gamble IF. Effects of formaldehyde on respriatory system. In: Gibson jE, ed. Formaldehyde toxicity. Washington, DC: Hemisphere Publishing Corporation, 1983; pp. 173-97.
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