Lung function and paper dust exposure among workers in a soft tissue paper mill

Occupational exposure to dust, both organic and inorganic, is clearly associated with lung function impairments and clinical outcomes like chronic obstructive pulmonary disease (COPD) and interstitial lung disease (Blanc et al. 2019). The pulp and paper industry is an important industrial sector in Sweden, and a large sector is the production of soft paper (FAO 2017). Growth in demand for particularly soft paper, i.e., toilet paper, paper towels, and napkins has been particularly strong in Asia (CEPI 2017). Soft paper mills still have high exposure to dust, and in previous decades, dust levels have frequently exceeded 10 mg/m³. Soft paper dust is an organic dust with a varying proportion of inorganic material depending on the use of additives (Sahle et al. 1990). In animal models, it has been shown that fibers from cellulose are biopersistent, and it has also been shown that exposure to cellulose dust are associated with fibrotic and granulomatous reactions (Muhle et al. 1997, Tatrai et al. 1996). Hence, it seems reasonable exposure to soft paper dust should be associated with impaired lung function.

We have in previous studies shown that high occupational exposure (> 5 mg/m³) to soft paper dust is associated with impaired lung function, mainly decreased forced expiratory volume in 1 s (FEV₁) and forced vital capacity (FVC) (Ericsson et al. 1988; Järvholm et al. 1988). A German study, also on soft paper mill workers with occupational exposure (> 5 mg/m³) to soft paper dust, observed a dose–response relationship for cumulative exposure to soft paper dust and decreased FVC (Kraus et al. 2004). By contrast, in two studies with lower exposure levels (≤ 5 mg/m³), there was no association between exposure to soft paper dust and lung function impairment (Heederik et al. 1987; Thorén et al. 1989b). There is also conflicting data about whether exposure to paper dust increases the risk for asthma and COPD (Thorén et al. 1989a; Torén et al. 1991, 1994, 1996). Hence, there is an obvious need for further studies investigating the relation between exposure to soft tissue paper dust and respiratory health effects, especially lung function outcomes.

In this study, we have examined workers in a large soft tissue paper mill in Sweden with the aim to elucidate the extent to which exposure to soft paper dust is associated with respiratory health effects.

All invited workers received an extensive questionnaire with questions about occupational history, smoking habits, and respiratory symptoms and asthma. Height and weight were measured with workers wearing light clothing and no shoes. Spirometry without bronchodilation was performed with a dry wedge spirometer (Vitalograph, Buckingham, UK) and according to American Thoracic Society (ATS)/European Respiratory Society (ERS) standards (Miller et al. 2005). Forced vital capacity and FEV₁ were measured with individuals in a sitting position and wearing a nose clip, and predicted normal values were based on the GLI-equations (Quanjer et al. 2012). Blood samples were analyzed for specific immunoglobulin E class using Phadiatop analysis (Pharmacia & Upjohn Diagnostics, Uppsala, Sweden).

One person was excluded due to inadequate spirometry technique; hence, the final study population comprised 198 workers with complete data regarding lung function and smoking habits. Basic data of the study population are shown in Table 2. In the univariate analyses, FEV₁ was significantly lower among the high exposed compared to the lower exposed workers, 91.4% vs. 97.8% predicted. Further, the prevalence of both AL_GOLD and AL_LLN was higher (p < 0.05) among the high exposed workers, 27.5% vs. 6.8%, and 19.6% vs. 6.1%, respectively.

In adjusted multiple linear regression models, lung function decreased for every high exposed year (Table 3). For each year of exposure to high levels of soft paper dust, there was a 0.87% predicted decrease in FEV₁ (95% CI − 1.39 to − 0.35). A similar, but lesser, effect was seen for FVC (− 0.54% predicted, 95% CI − 1.00 to − 0.08). Among never-smokers, the exposure effect was significant only with regard to FVC (− 1.33% predicted, 95% CI − 2.50 to − 0.16) (Table 3). Cumulative exposure to soft paper dust expressed as mg/m³-years was associated with decreased FEV₁ and decreased FVC (Table 3). This was seen among all workers and among ever-smokers. Among never-smokers the estimates also indicated decreased FEV₁ and FVC, but without formal statistical significance.

In the logistic regression models, high exposure to soft paper dust was associated with an increased odds ratio (OR) both for AL_GOLD (OR 4.6, 95% CI 1.8–12.0) for AL_LLN (OR 3.4, 95% CI 1.2–9.3) (Table 4). There were no significant associations with asthma, wheezing, or chronic bronchitis (Table 4).

The main finding from this study is that high exposure to soft paper dust (> 5.0 mg/m³) was associated with decreased pulmonary function. Previous studies have indicated restrictive lung function impairment associated with paper dust exposure; by contrast, the results from this study indicated obstructive impairment, as FVC was less affected than FEV₁, and the prevalence of AL was increased among high exposed workers.

Our previous study, showing a restrictive impairment of lung function, was conducted at paper mills with dust levels often exceeding 10 mg/m³; hence, probably higher than the exposure, present and past, at the mill in this study (Järvholm et al. 1988). In the present mill, the levels in the 1980s were between 5 and 10 mg/m³ total dust, but exposure levels were later reduced to around 1–2 mg/m³ (Thorén et al. 1989b). By analyzing the association between lung function and high exposed years, we consider both the intensity and the duration of exposure (De Vocht et al. 2015). Our findings in the present study indicate that working for at least 1 year at dust levels exceeding 5.0 mg/m³ is associated with significant lung function impairment. Such high exposure levels have not been present in the mill in the last two decades; hence, the affected workers have had quite a long exposure to soft paper dust. However, low exposed workers with a similar duration of exposure did not show any signs of lung function impairment. Among never-smokers FVC was significantly decreased, − 1.30% predicted but FEV₁ was not significantly affected.

Chronic airflow limitation (CAL), is commonly defined as an FEV₁/FVC ratio of < 0.7 (Vogelmeier et al. 2017). This has been seriously challenged, however, because the fixed ratio FEV₁/FVC < 0.7 does not take into account the age-related changes in lung function. Thus, it has been argued that employing a definition based on FEV₁/FVC < 0.7 leads to an overestimation of airflow limitation in the older population (Pellegrino et al. 2005). An alternative approach that has been proposed is to use the LLN as a cut-off. The LLN is calculated using the distribution in reference material; the use of LLN has been proposed by the ATS/ERS (Pellegrino et al. 2005). However, as we only had access to spirometry without bronchodilation, we analyzed AL as a proxy for CAL. However, we observed, as expected, that the prevalence of AL_GOLD was higher (12.1%) than the prevalence of AL_LLN (9.6%).

We decide to present both AL_GOLD and L_LLN as a joint American Thoracic Society/European Respiratory Society (ATS/ERS) statement called for investigations of comparisons between the fixed cut-off (FEV₁/FVC < 0.7) and the LLN-based definition (FEV₁/FVC < LLN) of airflow limitation in predicting adverse health outcomes (Celli et al. 2015). Our results also indicated that both definitions predicted an adverse outcome.

Whether soft paper dust exposure increases obstructive lung disease risk is unclear. Among soft tissue paper workers, we have previously described increased mortality due to obstructive lung disease as well as an insignificantly increased incidence rate of asthma (Thorén et al. 1989a; Torén et al. 1994). In addition, soft paper workers seem to have an increased prevalence of rhinitis and irritative symptoms of the upper airways, even those exposed to levels below 5 mg/m³ (Thorén et al. 1989b; Hellgren et al. 2001; Kraus et al. 2002, Holm et al. 2011). Among more highly exposed workers, increased prevalence of cough has been reported (Torén et al. 1994; Kraus et al. 2002). A suspected case of occupational asthma due to cellulose has also been described (Knight et al. 2018). Our results provide further evidence that high exposure to soft paper dust has irritating effects on the airways, impairs lung function and increases the risk for AL, regardless of how this is defined. In a longer perspective exposure to soft paper dust may also increase the risk for COPD (Järvholm 2000).

We also intended to define a group of workers with restrictive spirometric pattern, but the prevalence was too low to perform any meaningful analyses.

The present study has a number of methodological limitations that have to be considered. The main limitation is the cross-sectional design. This design implies that workers with long-standing respiratory ailments may have left the mill. We have previously shown that subjects with asthma or respiratory symptoms have an increased frequency of job change (Torén et al. 2009). This turnover of workers will cause an underestimation of the risk associated with paper dust exposure, due to healthy worker selection bias (Östlin 1989). The reference group in the present study was not unexposed; rather, they were low exposed workers, which may also have resulted in underestimation.

Our analysis adjusted for current smoking and cumulative dose of tobacco (pack-years). There is, however, a strong relation between decreased FEV₁ and increased prevalence of AL and tobacco smoking, and, hence, residual confounding by smoking cannot be excluded.

Another major limitation is the lack of power. The study size was limited to the workforce in one mill, which limited the number of study subjects. Still, there were significant associations between exposure and the lung function parameters.

The present study shows that occupational exposure to soft paper dust (years exceeding 5 mg/m³ total dust) is associated with lung function impairment and increased prevalence of obstructive lung function impairment.