Proximity to pulp and paper mills and wheezing symptoms among adolescents in North Carolina

Abstract

Using data from the North Carolina School Asthma Survey about the respiratory health of 64,432 adolescents attending public schools in North Carolina and data provided by school employees about the environmental health conditions of the school buildings, we assessed the prevalence of daytime wheezing during the past year among students estimated to be exposed to air pollutants arising from pulp and paper mills located near the schools. Of the schools the students attended, 14% (37/266) were located within 30 miles of one or more pulp and paper mills and odor from the mills was identified by survey respondents for 9 of the 266 schools. The prevalences of daytime wheezing in smokers and nonsmokers with household cigarette smoke exposure were elevated among students attending schools located within 30 miles of a pulp and paper mill, compared to the prevalence among students attending schools located beyond 30 miles (≤10 miles, prevalence ratio (PR): 1.21, 95% confidence interval (95% CI): 0.99, 1.43; 10–≤30 miles, PR: 1.06, 95% CI: 0.96, 1.16) and among students attending schools with noticeable odor from a pulp and paper mill (PR: 1.12, 95% CI: 0.93, 1.31). These results indicate a possible association between paper mill location and wheezing symptoms among adolescents and suggest that community-based exposure to pulp and paper mill emissions may have a greater impact on smokers and individuals exposed to cigarette smoke in the home than on nonsmokers without such household exposure.

1. Introduction

Air emissions arising from pulp and paper mills are of particular concern because of the adverse health effects associated with exposure to volatile organic compounds, sulfur dioxide, nitrogen oxides, total reduced sulfur compounds (TRS), and other hazardous air pollutants released from the mills. Emissions from paper mills can produce strong odors in the communities in which they are located, where exposed populations include children, the elderly, people with respiratory conditions, and others who may be sensitive to air pollutants. Studies in occupational settings show that paper mill workers experience an excess of dermatitis and airway inflammation (Jungbauer et al., 2005; Toren et al., 1997; Haug et al., 2002; Toren and Blanc, 1997; Rylander et al., 1999). Currently, there is little research, particularly among children, about the potential health effects of chronic community-level exposures to air emissions from paper mills, including hydrogen sulfide (H₂S), a major malodorous emissions component. In a New Zealand community with chronic H₂S exposure arising from a natural, geothermal source, higher than expected incidence of hospitalization for respiratory diseases was observed (Bates et al., 2002). In Finland, respiratory symptoms were observed to increase following a major air release from a pulp and paper mill (Haahtela et al., 1992), and the prevalences of eye and nasal symptoms, cough, and headache were slightly higher among children living in two communities located near pulp and paper mills and chronically exposed to malodorous sulfur compounds than among children in an unexposed community (Marttila et al., 1994). In the US, ambient H₂S and TRS levels were measured in two communities that contain numerous nonpulp and paper mill facilities identified as point sources of TRS, and elevated numbers of hospital visits for respiratory diseases among children were observed on days following high TRS levels, compared to days following low levels (Campagna et al., 2004). In addition to health concerns, air emissions from pulp and paper mills have generated complaints about odor and concern about the health effects of the malodorous air (Deane and Sanders, 1977; Jonsson et al., 1975). We conducted this study to investigate whether school-based exposure to air emissions from a paper mill is associated with wheezing symptoms among adolescents ages 12–14.

2. Materials and methods

During the 1999–2000 school year, the North Carolina Department of Health and Human Services conducted a statewide respiratory health surveillance project to assess the prevalence of respiratory symptoms among middle-school-aged children (Sotir et al., 2003). Approximately 67% (128,568/192,248) of all eligible students participated in the survey, which was implemented using an adapted version of the International Study of Asthma and Allergies in Childhood questionnaire, which combined a traditional written questionnaire with a series of video scenes showing children with asthma symptoms (Yeatts et al., 2000, 2003). Student participants in the survey provided information about their respiratory symptoms, including whether they had experienced wheezing symptoms during the day within the past year (i.e., “daytime wheezing”). Daytime wheezing was assessed when participants watched a video scene showing a child experiencing wheezing symptoms and responded to a written survey question about whether they had experienced symptoms like those shown in the video, within the past year (yes/no). Each student also provided information about his/her sex, age, race, allergies, socioeconomic status, cigarette smoking history, and home environment. We included age as a continuous variable (centered at 13) and categorized all other variables: race (black/white/other race); allergies to cat, dog, dust, grass, or pollen (yes/no); ever smoked cigarettes (yes/no); number of other smokers in household (none, 1, 2, 3+); and use of a gas stove at home (less than one time per month/1+times per month). Socioeconomic status was assessed using responses to a question about payment for lunch at school, with lower economic status designated by receiving free or reduced-price lunch at school compared to paying full price for lunch or bringing lunch to school.

Additional data for this study were collected for previous research about environmental triggers of asthma-related symptoms among adolescents in North Carolina (submitted for publication). During the 2003–2004 school year, we mailed four copies of a survey to principals of 337 public schools that participated in NCSAS and asked each principal to distribute the surveys to current school employees. Over 800 anonymous survey respondents, employed in 266 (79%) of the targeted schools, returned completed surveys and responded to questions about their observations of the environmental conditions in and around the school buildings. The survey did not include any questions about pulp and paper mills specifically; therefore all respondents who indicated that their schools are affected by odor from the mills did so without prompting. Odor from pulp and paper mills was reported in response to any of three open-ended questions soliciting information. The first opportunity was the last of a series of questions about odor arising from industries, including agriculture, landfills, and sewage treatment: “How often do you notice odor from another source, not yet mentioned, outside or inside the school building(s).” Respondents reporting odor from another source were asked “What is the source of the odor?” The second open-ended question asked “Do you ever hear staff or students talk about indoor or outdoor environmental odor? If yes, what is the source of the odor?” The final question was a completely open-ended survey question: “If there is anything else you want to tell us about the environmental conditions at your school please do so here.”

Three pulp mill emission exposure measures were created. First, each school’s exposure status was assigned according to distance between the school and the nearest pulp and paper mill; distances were calculated using latitude and longitude coordinates of the schools and the paper mills and were categorized (≤10 miles, >10–≤30 miles, >30 miles). A second measure was created by classifying schools for which any survey respondent identified noticeable odor from a paper mill as potentially exposed to air pollution from a pulp and paper mill. We created a third metric, based on both distance and odor, to compare schools located within 10 miles and with reported odor to schools located beyond 30 miles and without reported odor. When analyses were restricted to consider exposure to each of the four pulp and paper mills separately, schools located within 30 miles of each pulp and paper mill were compared to schools not located within 30 miles of any of the remaining mills.

From the 266 schools that participated in the school environmental health survey, the 64,432 boys and girls ages 12–14 who responded to NCSAS and provided complete data for all asthma survey variables of interest constitute our final study population. Based on findings of an occupational study that suggests larger respiratory effects of paper mill exposures among nonsmoking workers (Haug et al., 2002), we conducted analyses for individuals who reported currently, ever smoking, or never smoking but living with one or more smokers (“smokers+nonsmokers with household cigarette smoke exposure,” n = 39, 644) and those who reported never smoking and living with no smokers (“nonsmokers with no household cigarette smoke exposure,” n = 24, 788).

To assess the relationship between the prevalence of wheezing during the past year and the metrics of in-school exposure we used random-intercepts binary regression. This method accounted for the hierarchical clustering of student-level data within schools. Specifically, we used a variation of the generalized linear mixed model E(Y|x) = exp (α + Σ βx), similar to those described by Singer (1998) and McLeod (2001) in which the student’s outcome is modeled by a combination of student- and school-level equations. Student-level equations included variables for sex, age, race, economic status, allergy status, and use of a gas kitchen stove at home. The school-level equations included main exposure variable(s) and indicator variables for rural school locale and location within 3 miles of one or more confined swine feeding operations (submitted for publication). Associations between daytime wheeze and each metric of estimated exposure to air pollution from paper mills were estimated as prevalence ratios (PRs) using SAS 8.2 (SAS Institute, Inc., Cary, NC, USA).

3. Results

Over 13% (8417/64,432) of the boys and girls ages 12–14 reported daytime wheezing symptoms during the past year. The prevalence of wheezing was 17.9% among the 19,535 students who reported smoking, 12.4% among the 20,109 nonsmokers who reported sharing a home with one or more cigarette smokers, and 9.5% among the 24,788 nonsmokers with no household cigarette smoke exposure. Thirty-seven schools (14%) were located within 30 miles of one or more pulp and paper mills (Fig. 1). Odor from the mills was identified by survey respondents at 9 of the 266 schools, including 50% (4/8) of schools located within 10 miles of a pulp and paper mill, 14% (4/29) of schools located >10–≤30 miles, and <1% (1/229) of schools located beyond 30 miles of the nearest mill. Distances between the schools for which odor was identified by survey respondents and each school’s nearest pulp and paper mill ranged from 1.9 to 35 miles.

Fig. 1.

Locations of 266 public schools and four paper mills in North Carolina. Diamonds indicate public schools. Stars represent pulp and paper mills. The inner circles represent 10 mile buffers and the outer circles represent 30 mile buffers. Solid lines show county boundaries. Schools located in 14 western North Carolina counties were excluded from data collection based on the aims of the study for which the data were collected. One paper mill located in the excluded region and with no surveyed schools located within 30 miles was excluded.

Table 1 shows the associations, stratified by smoking status and exposure to second-hand cigarette smoke, of daytime wheeze during the past year with distance to the nearest pulp and paper mill, reported odor, and the metric created using a combination of distance categories and survey-based odor information. Among smokers and nonsmokers who reported sharing a home with one or more cigarette smokers, the prevalences of daytime wheezing were elevated in schools located within 30 miles of a pulp and paper mill, compared to the prevalences in schools located beyond 30 miles, and the PRs declined with distance (Table 1). Elevated prevalences were also observed among students attending schools with reported odor from a pulp and paper mill, compared to students attending schools without any such odor. Highest PRs were generated for comparisons of the prevalence of wheezing among all students attending schools located within 10 miles of a pulp and paper mill and with reported odor, compared to the prevalence among students attending schools located beyond 30 miles and without reported odor (PR: 1.23, 95% CI: 0.95, 1.51). For each of the exposure metrics, including the distance- and odor-based measure, the directions and magnitudes of the effects were similar for the subgroups of students identified as smokers and nonsmokers with household cigarette smoke exposure. Among smokers attending schools located within 10 miles of a pulp and paper mill and with reported odor, the prevalence of daytime wheezing was 25% higher, compared to the prevalence among smokers attending schools located beyond 30 miles and without reported odor (PR: 1.25, 95% CI: 0.89, 1.61); among nonsmokers with household cigarette smoke exposure prevalence of daytime wheezing was 34% higher among students in exposed schools, compared to unexposed schools (PR: 1.34, 95% CI: 0.87, 1.81). Using this distance- and odor-based estimate of exposure, when analyses were restricted to consider exposure to air pollutants from each of the four pulp and paper mills separately, PRs ranged from 1.20 (95% CI: 0.75, 1.66) to 1.41 (95% CI: 0.61, 2.22), in the population of smokers and nonsmokers with household cigarette smoke exposure, and 0.91 (95% CI: 0.24, 1.58) to 1.14 (95% CI: 0.09, 2.18) among nonsmokers with no household cigarette smoke exposure.

Table 1.

Associations of distance to and odor from pulp and paper mills with daytime wheeze in the past year among students attending 266 public schools in North Carolina

Exposure measure	No. schools	All students			Smokers+nonsmokers with household cigarette smoke exposure			Nonsmokers with no household cigarette smoke exposure
		No. students	% Wheeze	PR (95% CI)a	No. students	% Wheeze	PR (95% CI)a	No. students	% Wheeze	PR (95% CI)b
Distance to paper mill
0–≤10 miles	8	1381	15.1	1.15 (0.96, 1.34)	854	19.3	1.21 (0.99, 1.43)	527	8.2	0.93 (0.67, 1.20)
>10–≤30 miles	29	5859	14.9	1.03 (0.94, 1.12)	3785	17.9	1.06 (0.96, 1.16)	2074	10.1	0.94 (0.81, 1.08)
>30 miles	229	57,192	12.6	1.00	35,005	14.7	1.00	22,187	9.4	1.00
Survey-reported odor
Odor report	9	1886	14.7	1.11 (0.94, 1.28)	1215	17.5	1.12 (0.93, 1.31)	671	9.5	1.04 (0.79, 1.30)
No odor report	257	62,546	12.8	1.00	38,429	15.0	1.00	24,117	9.5	1.00
Distance/odor classification
0–≤10 miles+odor report	4	718	15.9	1.23 (0.95, 1.51)	484	19.1	1.28 (0.97, 1.58)	234	8.6	1.02 (0.60, 1.44)
>30 miles+no odor report	228	56,854	12.6	1.00	34,786	14.7	1.00	22,068	9.4	1.00

^aAdjusted for sex, age, race, subsidized lunch, allergies, ever smoked cigarettes, number of other cigarette smokers in household, gas stove at home, rural locale, and location within 3 miles of a confined swine feeding operation.

^bAdjusted for sex, age, race, subsidized lunch, allergies, gas stove at home, rural locale, and location within 3 miles of a confined swine feeding operation.

4. Discussion

We found associations between proximity to a pulp and paper mill and elevated prevalence of daytime wheezing among students who reported using cigarettes or experiencing second-hand cigarette smoke exposure. Stratification of our analysis by smoking status and cigarette smoke exposure was driven by previous research that reported elevated associations between occupational exposure to culturable microorganisms and respiratory cough, dyspnea, gastrointestinal symptoms, skin rash, and other symptoms among workers in a paper mill and specifically reported that the association of respiratory cough was slightly higher among nonsmoking workers (Haug et al., 2002). In contrast, our results suggest that environmental exposures may have a greater impact on children who smoke or are exposed to cigarette smoke in the home than on other children. Exposure to tobacco smoke could increase sensitivity to low levels of other respiratory irritants. The large proportions of middle school students in this survey who reported ever or currently smoking (30%) or never smoking but living in a household with smokers (31%) indicate that tobacco exposure is a major public health concern for adolescents in North Carolina.

Our study offers a preliminary assessment of one potential adverse health effect of exposure to hazardous air pollutants from pulp and paper mills. Although the magnitudes of the association between daytime wheezing and attending schools located near paper mills are small, the public health consequences of these exposures are of concern due to the high prevalence of wheezing and the negative medical, behavioral, and educational consequences of asthma among adolescents. Use of a standardized questionnaire to assess wheezing and independent measures of exposure and outcome are strengths of this study. The lack of physical measures of exposures at schools and individual measures of students’ exposures away from school are major weaknesses. Misclassification of exposure likely limits the ability of this study to detect an effect of exposure. Publicly available data about hazardous air pollutants released from each of the four mills indicate that the total point source and fugitive air emissions include sulfur dioxide, carbon disulfide, dimethyl sulfide, and other pollutants known to affect the respiratory tract (US EPA, 2005). In our data, PRs for distance-and odor-based estimates of exposure to the individual paper mills vary only slightly, whereas the released quantities of each air pollutant vary widely; we did not observe an association between estimated releases of any specific hazardous air pollutant and the prevalence of daytime wheezing.

Despite the limitations of our study design and, in particular, despite the lack of more specific measures of exposure to pulp and paper mill emissions, our findings indicate a higher prevalence of wheezing among children ages 12–14 attending schools located near pulp and paper mills. The association is limited to children whose respiratory tracts may be vulnerable to environmental irritants due to their personal cigarette smoking experience or the habits of their family members, suggesting the importance of considering interactions between environmental exposures and personal or household exposures in assessing the impacts of hazardous air pollutants on children’s respiratory health. Better assessment of community exposures to H₂S and other emissions would improve research into the potential health impacts of hazardous air pollutants from pulp and paper mills on vulnerable neighboring populations.