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(Chest. 2004;125:731-736.)
© 2004 American College of Chest Physicians

Lung Function Among Workers in the Soft Tissue Paper-Producing Industry*

Thomas Kraus, MD; Annette Pfahlberg, PhD; Petra Zöbelein, MD; Olaf Gefeller, PhD and Hans Jürgen Raithel, MD, PhD

* From the Institute and Outpatient-Clinic for Occupational Medicine (Dr. Kraus), University Hospital, Aachen University of Technology, Aachen; and Department of Medical Informatics, Biometry and Epidemiology (Drs. Pfahlberg and Gefeller), and Institute and Outpatient-Clinic for Occupational, Social and Environmental Medicine (Drs. Zöbelein and Raithel), University of Erlangen-Nuremberg, Erlangen, Germany.

Correspondence to: Thomas Kraus, MD, Institute and Outpatient-Clinic for Occupational Medicine, University Hospital, Aachen University of Technology, Pauwelsstr. 30 D-52074, Aachen, Germany; e-mail: thomas.kraus{at}post.rwth-aachen.de


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objectives: To describe lung function in correlation with information on exposure to dust and fibers in soft tissue paper-producing factories in Germany.

Methods: Ambient monitoring was performed for inhalable, respirable dust and fibers in nine soft tissue paper-producing factories. In a study group of 1,047 workers (189 control subjects, 240 workers with moderate exposure, and 618 workers with high exposure), spirometry (FVC, FEV1) was performed. Information on occupational history, duration of exposure, workshop within the company, former occupational exposures, and smoking habits were collected. By employing multiple linear regression modeling, the potentially confounding effects of age, sex, body mass index, smoking habits, and factory were incorporated into the analysis of FVC, FEV1, and FEV1 in percent of FVC (FEV1%FVC). By employing a logistic regression model, odds ratios were calculated for FVC < 80% predicted in different exposure subgroups.

Results: The mean concentrations for inhalable, respirable, and fibrous dusts were 12.4 mg/m3, 0.28 mg/m3, and 420,000 fibers per cubic meter. With relation to cumulative dust and fiber exposure, a decrease of FVC from 105.4% predicted to 96.9% predicted (dust) and 97.1% predicted (fibers) in the subgroup with highest cumulative exposure was observed. For FEV1, a decrease from 107.3% predicted to 103.0% predicted (dust) and 102.8% predicted (fibers) was found. The parameter estimates show dose-response relationships that are more pronounced for FVC compared to FEV1. FEV1%FVC did not change significantly with increasing cumulative exposure, indicating a restrictive pattern of the findings.

Conclusions: Due to high ambient dust concentrations and the observed adverse effects on lung function, a reduction of dust exposure and secondary preventive measures is advised.

Key Words: cellulose fibers • cumulative exposure index • occupation


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
In the pulp and paper-producing industry, workers are exposed to a wide variety of hazardous substances.1 2 3 Due to the possible adverse effects on human lungs, fiber-containing dusts are of special interest in occupational medicine. Animal experiments with cellulose fibers and cellulose fiber products (Isofloc; Ökologische Bautechnik; Hess. Lichtenan, Germany) showed a relatively high biopersistence. Moreover, granulomatous pneumonia and minimal interstitial fibrosis as well as alveolar cell-type hyperplasia were found in rats.4 5 6 7

In the literature, there is limited evidence for an increased prevalence of respiratory symptoms in paper workers. Some authors8 9 10 11 described adverse effects on lung function; however, the intensity and type of the reported effects have been inconsistent. While some authors12 13 14 found a more obstructive pattern, others10 described a decreased lung elastic recoil pressure and decreased residual volume. Due to multiple exposure to substances including chemicals, ozone, and fiber-containing dusts, the mechanisms that are responsible for these effects and the causal relationships with certain exposures could not yet be described.15

The aim of our study was therefore to evaluate the potential impact of exposure to these substances on lung function of workers employed in nine soft tissue plants in Germany. These findings were correlated with information on the corresponding dust and fiber exposure and smoking habits.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
The study group was recruited from soft tissue paper-producing companies from different parts of Germany. In every company, pure cellulose was the main basis of the production process. Recycled paper was not a relevant component of the products.

Work Process
At first, cellulose is put into pulping machines and high amounts of water are added. The pulp is then brought into huge paper machines, where the dehydrating and drying process is performed. The result of this process are so-called "mother rolls" (huge paper rolls). Afterwards, the converting process begins with printing and cutting the product in combiner machines. Finally the soft tissue products are packed. During this production process, high dust concentrations appear especially at the paper machine and during the converting process, depending on the location and activity taking place.

Study Population
The study group comprised all persons working in the production unit of nine randomly chosen companies. There was no selection based on exposure intensity, size of the factories, health complaints among employees, or other factors. Data were collected from 1,047 persons. According to the employers’ information, we examined all persons from the different workshops employed at the time period 1996/1998. However, we had no possibility to check the list of all persons employed and to compare them with the list of persons we examined. Characteristics of the study group are presented in Table 1 .


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  		Table 1.. Number, Age, Sex, Smoking Habits, and Duration of Exposure in Workers*

 
The data concerning dust measurements were gathered from 1991 to 1997. Dust measurements were performed according to the Technical Guidelines for the Detection and Measurement of Hazardous Substances.16 The mean sampling time was 1.97 h (range, 0.16 to 3.8 h). The cross-sectional study with the data collection concerning lung function, occupational history, and smoking habits took place in the years from 1996 to 1998. Three subgroups were defined within the study group. Group 1 consists of control persons of each company from the management departments. Group 2 had moderate exposure (maintenance workers, electricians, mechanics). Group 3 consists of workers from the production workshops (paper machine, combiner) and was classified as having high exposure. Due to differences in the exposure intensity between the nine companies, a cumulative exposure index was generated for describing the individual exposure. The mean of the dust and fiber concentrations of each company were multiplied by the individual time of exposure of persons with high exposure. In cases of moderate exposure, the mean dust and fiber concentrations of each company was divided by four and multiplied by the individual time of exposure. According to the information from technical experts, this attenuation factor best represents the intermittent and lower exposure of those workers. For each participant, a cumulative exposure index was available for dust and for fibers. Because dust measurements for the respirable fraction (diameter < 5 µm) was not available from each company, no exposure index was calculated for this fraction.

From all subjects, information on occupational history, duration of exposure, workshop within the company, former occupational exposures, and smoking habits were available. Informed written consent was obtained from each participant.

Spirometry was performed with a Jaeger-Masterlab (two companies, n = 606) and a Jaeger Flowscreen (n = 441) [Jaeger-Toennies; Würzburg, Germany] according to American Thoracic Society criteria.17 It included the measurement of the FVC and FEV1. Relative values were calculated for the measured lung function parameters by using the reference values proposed by the European Community for Coal and Steel.18

Descriptive data analysis for the parameters FEV1, FVC, and FEV1 in percent of FVC (FEV1%FVC) comprise the calculation of means and SDs of these parameters in exposure categories of cumulative dust and fiber exposure, respectively. The categorization of these variables into ordinal groups was based on a priori defined scheme of cut points. Moreover, number and percentage of FVC values < 80% predicted were calculated.

In a second step, the potentially confounding effects of factory, age, sex, body mass index, and smoking habits were incorporated into the analysis by employing multiple linear regression modeling. Separate regression models were set up for the lung function parameters FEV1, FVC, and FEV1%FVC, which were included untransformed as dependent variables into the model, because their empirical distribution was approximately normal. Parameter estimates from these models show the adjusted effects of the specific dust/fiber exposure category on the FEV1, FVC, and FEV1%FVC, respectively, relative to the control group. Statistical significance of these changes is assessed by the test within the regression model whether the corresponding model parameters equals 0.

In a third step, odds ratios and p values for the clinically relevant threshold FVC < 80% predicted were calculated for the different exposure subgroups in a logistic regression model incorporating factory, age, sex, body mass index, and smoking habits. All reported p values are two sided, those < 0.05 were considered as significant. The statistical analyses were performed using the SPSS version 10 (SPSS; Chicago, IL) and SAS version 8.1 (SAS Institute; Cary, NC).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Ambient Monitoring
The results of the ambient monitoring of dust and fiber concentrations are presented in Table 2 . The mean concentrations for inhalable dusts were 12.4 mg/m3. Maximum concentrations found were 30 mg/m3 inhalable dust during the production process at the machines and 96 mg/m3 during cleaning the machines with pressured air. Measurements of the respirable dust fraction in five of nine companies yielded mean concentrations of 0.28 mg/m3 with a maximum of 1.78 mg/m3. The mean ratio of respirable to inhalable fraction was 4.5%. The maximum of the fiber concentrations was 1.5 million fibers per cubic meter. Mean fiber concentrations were 420,000 fibers/per cubic meter (Table 2) . The mean cumulative exposure index based on these ambient monitoring results and duration of exposure was 27.7 dust-years for workers with moderate exposure and 112.7 dust-years for workers from the production units. The corresponding results for fiber-years were 0.9 and 3.9, respectively.


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  		Table 2.. Ambient Monitoring for Inhalable, Respirable, and Fiber Concentrations*

 
Lung Function Analysis
With relation to cumulative dust exposure FEV1 decreased significantly in workers with > 25 dust-years from 107.3% (reference) to 101.0% predicted (Table 3 ). Corresponding results with FEV1 decrease of 5.2% were observed with relation to cumulative fiber exposure (Table 3) . The parameter estimates show a dose-response relationship, which is pronounced between the categories < 25 dust-years and 25 to 100 dust-years (Table 4 ). Cumulative exposure to < 3 fiber-years already leads to a significant reduction of FEV1 (Table 4) . Both evaluations showed a small increase of mean FEV1% predicted in the subgroup with the highest cumulative exposure (Table 3) .


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  		Table 3.. FEV1, FVC, FEV1%FVC, and No. and Percentage of Cases With FVC < 80% Predicted for Different Dust/Fiber-Exposure Categories and Smoking Status

 

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  		Table 4.. Results of Different Multiple Regression Models: Changes in Function Adjusted for Factory, Body Mass Index, Age, Sex, and Smoking Habits

 
For FVC, a dose-dependent decrease from 105.4 to 96.9% predicted in the subgroup with highest cumulative dust exposure was observed (Table 3) . This effect was also found with relation to cumulative fiber exposure (105.4% predicted and 97.1% predicted). The parameter estimates with relation to dust-years and fiber-years (Table 4) show clear dose-response relationships that are more pronounced compared to FEV1.

FEV1%FVC did not change significantly in the subgroups with different exposure intensity. The relation of both parameters slightly increased with increasing exposure intensity without reaching statistical significance (Tables 3 , 4) .

The prevalence of FVC < 80% predicted rose with increasing cumulative dose from 1.0% (reference) to 15.3% (dust) and 15.0% (fibers) in the subgroup with the highest cumulative exposure (Table 3) . The odds ratios increased significantly for cumulative dust exposure from 9.3 (<= 25 dust-years) to 11.7 (25 to 100 dust-years) to 16.3 (> 100 dust-years) and for cumulative fiber exposure from 11.4 (<= 3 fiber-years) to 17.4 (> 3 fiber-years) [Table 4 ].

Smoking habits had no significant effects on FVC, FEV1%FVC, and the prevalence of FVC < 80% predicted, but a significant effect on FEV1 (p = 0.0001) [Table 4 ]. Mean values of former smokers were similar to those of nonsmokers (106.7% predicted vs 105.9% predicted) [Table 3 ].


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Animal experiments suggest that cellulose fibers have a long biopersistence at least in rat lungs and can cause slight interstitial fibrosis, fiber-associated granulomata, alveolar histiocytosis, alveolar lipoproteinosis, as well as alveolar cell-type hyperplasia.4 5 6 7 Therefore, impaired lung function could be expected to be a plausible adverse effect after occupational soft tissue fiber and/or dust exposure. However, scientific reports on lung function analysis in soft tissue workers are contradictory and inconsistent. This might be due to small study groups and considerably differing exposure intensities. Cross-sectional studies in soft-tissue paper-producing factories with high exposure described a high prevalence of respiratory symptoms,8 9 and a decreased lung function in workers with at least 10 years of exposure to concentrations of paper dust > 5 mg/m3.9 In low-dose exposed workers, no adverse effects on lung function could be detected.11 19

It has been a matter of concern whether fiber shape of cellulose containing dusts might be responsible for health complaints and respiratory diseases with lung function impairment. Therefore, inhalable dust and fiber dust concentrations were determined in our study simultaneously. The results of the ambient monitoring revealed very high dust exposures for the inhalable dust fraction, whereas the respirable fraction was considerably low (Table 2) . This might lead to the suggestion that in our study the potential for the detection of adverse effects on the lower respiratory tract could be small.

However, a significant decrease of FVC of 8.5% was found with relation to cumulative dust and fiber exposure (8.3%). This effect was found despite a relatively low respirable dust fraction of 4.5% on average and after adjustment for important confounding factors. The parameter estimates show a dose-response relationship with relation to cumulative exposure indexes based on a high number of dust measurements. Moreover a significant decrease of FEV1 of 6.3% was found for workers with a cumulative exposure > 25 dust-years compared to the reference group. FEV1/FVC ratio is not significantly increased with increasing cumulative exposure. This indicates that a restrictive pattern of lung function impairment occurs with increasing cumulative exposure to soft tissue paper dust.

When interpreting the results of our study, it should be considered, that compared to other studies, very high dust exposure was detected on average exceeding the threshold limit value of 10 mg/m3.20 Due to these high exposures and due to the study design of a cross-sectional study, a healthy worker effect is likely to occur and might lead to an underestimation of the adverse effects described. Workers with manifest respiratory diseases and severe lung function impairment are not able to work under dusty conditions at paper machines or combiners.

The results of our study do not support the hypothesis that cellulose fiber exposure has a separate or specific effect on lung function. However, a clear separation of specific fiber and dust effects is not possible due to methodologic problems (different units). The interpretation has to take into account the fact that fibers are part of the total dust amount. The parameter estimates with relation to cumulative dust-years and fiber-years reveal similar results (Table 4) .

It is still unknown if the effects on lung function described in the literature and those found in this study are reversible or persistent. Some results from different exposure settings suggest that deterioration of lung function parameters is an across-shift effect that is reversible. Christiani et al21 described a link between across-shift decline of FEV1 and 5-year decline of FEV1 in cotton workers.21 Across-shift decline was predictive for chronic effects > 5 years. In our study, no information was available on across-shift changes of lung function. The analyses were performed within one shift. Further evidence for across-shift changes after organic dust exposure was found in a study in poultry workers. Exposure concentrations associated with significant across-shift pulmonary function decrements were 2.4 mg/m3 total dust, 0.16 mg/m3 respirable dust, 614 EU/m3 endotoxin, and 12 ppm ammonia.22 The dust concentrations were considerably lower than those in our study.

In our study, both FVC and FEV1 decreased with increasing exposure. FEV1%FVC did not change significantly, with only a slight increase showing that FVC decreased more than FEV1. Moreover, the prevalence of clinically relevant decreased FVC (< 80% predicted) rose with increasing exposure. This might be a sign of a restrictive pattern, which has not been described in the literature so far, and that could be due to early fibrotic effects. To clarify this question, lung volume measurements and chest radiograph or thin-section CT, which is more sensitive, would be helpful to detect possible interstitial disease.

In this context, it has also to be discussed whether dust and fiber concentrations in our study are surrogate markers for nondetected exposures at the workplaces. It is well known that in the soft tissue paper-producing industry, a complex exposure situation exists.2 3 Moreover lung function impairment has been reported from other work sites with organic dust exposure outside the soft tissue paper-producing industry, eg, among cotton textile workers and poultry workers.21 22 Lung function impairment could be unspecifically related to the very high dust concentrations no matter what kind of dust exposure takes place (overload phenomenon). Searching for the etiologic agent, Rylander et al14 described that airborne endotoxin and 1–3 ß glucan exposure were responsible for the increased prevalence of respiratory symptoms and for a decreased baseline FEV1 and an increased airway responsiveness in a group of 83 workers employed in bark-cleaning units, recycled paper storage, and processing in the paper industry. This exposure is not comparable with soft tissue paper production. Recycled paper and recycled paper dust and fibers have different properties (eg, diminished fiber length) than soft tissue paper dust. Moreover, dust concentrations are higher in the soft tissue paper production. Due to the results of the markers of inflammation determined in the study by Rylander et al,14 it has to be discussed whether airway inflammation is responsible for the lung function findings.14 However, the responsible agent still remains unclear. Douwes et al23 described in their study from saw mills that dust levels were only weakly correlated with endotoxin and 1,3 ß glucan levels. Therefore, it is questionable if the dust concentrations detected in our study can serve as a surrogate for endotoxin exposures. All in all, most of the results suggest that the effects detected are unspecific due to the high dust concentrations regardless of its fiber content and probably regardless of other undetected exposures.

Therefore, a reduction of dust exposures is recommended in the soft tissue paper-producing industry. In order to allow specific evidence-based prevention, further investigation is needed to identify the etiologic agent or agents within the dust fraction.


   Acknowledgements
 
We thank all occupational health physicians from the participating companies, and special thanks to Kathy Bischof for editorial assistance.


   Footnotes
 
Abbreviation: FEV1%/FVC = FEV1 in percent of FVC

This study was supported by a grant from the Papiermacher-Berufsgenossenschaft.

Received for publication October 16, 2002. Accepted for publication June 10, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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