Exposures to numerous substances designated by the International Agency for Research on Cancer (IARC) as known, probable and possible carcinogens may occur in pulp and paper operations. Asbestos, known to cause lung cancer and mesothelioma, is used to insulate pipes and boilers. Talc is used extensively as a paper additive, and can be contaminated with asbestos. Other paper additives, including benzidine-based dyes, formaldehyde and epichlorohydrin, are considered probable human carcinogens. Hexavalent chromium and nickel compounds, generated in stainless-steel welding, are known lung and nasal carcinogens. Wood dust has recently been classified by IARC as a known carcinogen, based mainly on evidence of nasal cancer among workers exposed to hardwood dust (IARC, 1995). Diesel exhaust, hydrazine, styrene, mineral oils, chlorinated phenols and dioxins, and ionizing radiation are other probable or possible carcinogens which may be present in mill operations.

Few epidemiological studies specific to pulp and paper operations have been conducted, and they indicate few consistent results. Exposure classifications in these studies have often used the broad industrial category “pulp and paper”, and even the most specific classifications grouped workers by types of pulping or large mill areas. The three cohort studies in the literature to date involved fewer than 4,000 workers each. Several large cohort studies are currently under way, and IARC is coordinating an international multicentric study likely to include data from more than 150,000 pulp and paper workers, allowing much more specific exposure analyses. This article will review the available knowledge from studies published to date. More detailed information may be obtained from earlier published reviews by IARC (1980, 1987, and 1995) and by Torén, Persson and Wingren (1996). Results for lung, stomach and haematological malignancies are summarized in table 1.

Table 1. Summary of studies on lung cancer, stomach cancer, lymphoma and leukaemia in pulp and paper workers

C = cohort study, CR = case-referent study, PM = proportionate mortality study.
* Statistically significant. ^§ = Where separately reported, NHL = non Hodgkin lymphoma and HD = Hodgkin’s disease. X = 0 or 1 case reported, no risk estimate calculated, — = No data reported.

A risk estimate exceeding 1.0 means the risk is increased, and a risk estimate below 1.0 indicates decreased risk.

Source: Adapted from Torén, Persson and Wingren 1996.

Respiratory System Cancers

Maintenance workers in paper and pulp mills experience an increased risk of lung cancer and malignant mesotheliomas, probably because of their exposure to asbestos. A Swedish study showed a threefold increased risk of pleural mesothelioma among pulp and paper workers (Malker et al. 1985). When the exposure was further analysed, 71% of the cases had been exposed to asbestos, the majority having worked in mill maintenance. Elevations in lung cancer risk among maintenance workers have also been shown in Swedish and Finnish pulp and paper mills (Torén, Sällsten and Järvholm 1991; Jäppinen et al. 1987).

In the same Finnish study, a twofold increased risk of lung cancer was also observed among both paper mill and board mill workers. The investigators made a subsequent study restricted to pulp mill workers exposed to chlorine compounds, and found a threefold increased risk of lung cancer.

Few other studies of pulp and paper workers have shown increased risks for lung cancer. A Canadian study showed an increased risk among those exposed to paper dust (Siemiatycki et al. 1986), and US and Swedish studies showed increased risks among paper mill workers (Milham and Demers 1984; Torén, Järvholm and Morgan 1989).

Gastro-intestinal Cancers

Increased risk of stomach cancer has been indicated in many studies, but the risks are not clearly associated with any one area; therefore the relevant exposure is unknown. Socio-economic status and dietary habits are also risk factors for stomach cancer, and might be confounders; these factors were not taken into account in any of the studies reviewed.

The association between gastric cancer and pulp and paper work was first seen in a US study in the 1970s (Milham and Demers 1984). The risk was found to be even higher, nearly doubled, when sulphite workers were examined separately. US sulphite and groundwood workers were also found in a later study to run an increased risk of stomach cancer (Robinson, Waxweiller and Fowler 1986). A risk of the same magnitude was found in a Swedish study among pulp and paper mill workers from an area where only sulphite pulp was produced (Wingren et al. 1991). American paper, paperboard and pulp mill workers in New Hampshire and Washington state ran an increased mortality from stomach cancer (Schwartz 1988; Milham 1976). The subjects were probably a mixture of sulphite, sulphate and paper mill workers. In a Swedish study, threefold increased mortality due to stomach cancer was found in a group comprising sulphite and paper mill workers (Wingren, Kling and Axelson 1985). The majority of pulp and paper studies reported excesses of stomach cancer, though some did not.

Due to the small number of cases, most studies of other gastrointestinal cancers are inconclusive. An increased risk of colon cancer among workers in the sulphate process and in paper board production has been reported in a Finnish study (Jäppinen et al. 1987), as well as among US pulp and paper workers (Solet et al. 1989). The incidence of biliary tract cancer in Sweden between 1961 and 1979 was linked with occupational data from the 1960 National Census (Malker et al. 1986). An increased incidence of cancer of the gallbladder among male paper mill workers was identified. Increased risks of pancreatic cancer have been observed in some studies of paper mill workers and sulphite workers (Milham and Demers 1984; Henneberger, Ferris and Monson 1989), as well as in the broad group of pulp and paper workers (Pickle and Gottlieb 1980; Wingren et al. 1991). These findings have not been substantiated in other studies.

Haematological Malignancies

The issue of lymphomas among pulp and paper mill workers was originally addressed in a US study from the 1960s, where a fourfold increased risk of Hodgkin’s disease was found among pulp and paper workers (Milham and Hesser 1967). In a subsequent study, the mortality among pulp and paper mill workers in the state of Washington between 1950 and 1971 was investigated, and a doubled risk of both Hodgkin’s disease and multiple myeloma was observed (Milham 1976). This study was followed by one analysing mortality among pulp and paper union members in the United States and Canada (Milham and Demers 1984). It showed almost a threefold increased risk for lymphosarcoma and reticulum cell sarcoma among sulphite workers, while sulphate workers had a fourfold increased risk of Hodgkin’s disease. In a US cohort study, sulphate workers were observed to have a twofold risk of lymphosarcoma and reticulosarcoma (Robinson, Waxweiller and Fowler 1986).

In many of the studies where it was possible to investigate the occurrence of malignant lymphomas, an increased risk has been found (Wingren et al. 1991; Persson et al. 1993). Since the increased risk occurs both in sulphate and sulphite mill workers, this points towards a common source of exposure. In the sorting and chipping departments, the exposures are rather similar. The workforce is exposed to wood dust, terpenes and other extractable compounds from the wood. In addition, both pulping processes bleach with chlorine, which has the potential to create chlorinated organic by-products, including small amounts of dioxins.

Compared with lymphomas, studies on leukaemias show less consistent patterns, and the risk estimates are lower.

Other Malignancies

Among US paper mill workers with presumed exposure to formaldehyde, four cases of urinary tract cancer were found after 30 years’ latency, although only one was expected (Robinson, Waxweiller and Fowler 1986). All of these individuals had worked in the paper-drying areas of the paper mills.

In a case-control study from Massachusetts, central nervous system tumours in childhood were associated with an unspecified paternal occupation as a paper and pulp mill worker (Kwa and Fine 1980). The authors regarded their observation as a random event. However, in three subsequent studies, increased risks were also found (Johnson et al. 1987; Nasca et al. 1988; Kuijten, Bunin and Nass 1992). In studies from Sweden and Finland, two- to threefold increased risks of brain tumours were observed among pulp and paper mill workers.

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Injuries

Only limited statistics are available on accident rates in general in this industry. Compared to other manufacturing industries, the 1990 accident rate in Finland was below the average; in Canada, the rates from 1990 to 1994 were similar to other industries; in the United States, the 1988 rate was slightly above average; in Sweden and Germany, the rates were 25% and 70% above the average (ILO 1992; Workers’ Compensation Board of British Columbia 1995).

The most commonly encountered risk factors for serious and fatal accidents in the pulp and paper industry are the papermaking equipment itself and the extreme size and weight of pulp or paper bales and rolls. In a 1993 United States government study of occupational fatalities from 1979 to 1984 in pulp, paper and paperboard mills (US Department of Commerce 1993), 28% were due to workers being caught in or between rotating rolls or equipment (“nip-points”) and
18% were due to workers being crushed by falling or tumbling objects, especially rolls and bales. Other causes of multiple deaths included electrocution, hydrogen sulphide and other toxic gas inhalation, massive thermal/chemical burns and one case of heat exhaustion. The number of serious accidents associated with paper machines has been reported to decrease with the installation of newer equipment in some countries. In the converting sector, repetitive and monotonous work, and the use of mechanized equipment with higher speeds and forces, has become more common. Although no sector-specific data are available, it is expected that this sector will experience greater rates of over-exertion injuries associated with repetitive work.

Non-Malignant Diseases

The most well documented health problems encountered by pulp mill workers are acute and chronic respiratory disorders (Torén, Hagberg and Westberg 1996). Exposure to extremely high concentrations of chlorine, chlorine dioxide or sulphur dioxide may occur as a result of a leak or other process upset. Exposed workers may develop acute chemical-induced lung injury with severe inflammation of air passages and release of fluid into the air spaces, requiring hospitalization. The extent of damage depends on the duration and intensity of the exposure, and the specific gas involved. If the worker survives the acute episode, complete recovery may occur. However, in less intense exposure incidents (also usually as a result of process upsets or spills), acute exposure to chlorine or chlorine dioxide may trigger the subsequent development of asthma. This irritant-induced asthma has been recorded in numerous case reports and recent epidemiological studies, and current evidence indicates that it may persist for many years following the exposure incident. Workers similarly exposed who do not develop asthma may experience persistently increased nasal irritation, cough, wheezing and reduction in airflow rates. Workers most at risk for these exposure incidents include maintenance workers, bleach plant workers and construction workers at pulp mill sites. High levels of chlorine dioxide exposure also cause eye irritation and the sensation of seeing halos around lights.

Some mortality studies have indicated increased risk of death from respiratory disease among pulp mill workers exposed to sulphur dioxide and paper dust (Jäppinen and Tola 1990; Torén, Järvholm and Morgan 1989). Increased respiratory symptoms have also been reported in sulphite mill workers who are chronically exposed to low levels of sulphur dioxide (Skalpe 1964), although increased airflow obstruction is not normally reported among pulp mill populations in general. Symptoms of respiratory irritation are also reported by workers exposed to high air concentrations of terpenes in turpentine recovery processes often present at pulp mill sites. Soft paper dust has also been reported to be associated with increased asthma and chronic obstructive pulmonary disease (Torén, Hagberg and Westberg 1996).

Exposure to micro-organisms, especially around wood chip and waste piles, debarkers and sludge presses, creates an increased risk for hypersensitivity responses in the lungs. Evidence for this appears to be limited to isolated case reports of hypersensitivity pneumonitis, which can lead to chronic lung scarring. Bagassosis, or hypersensitivity pneumonitis associated with exposure to thermophylic micro-organisms and bagasse (a sugar cane by-product), is still seen in mills using bagasse for fibre.

Other respiratory hazards commonly encountered in the pulp and paper industry include stainless steel welding fumes and asbestos (see “Asbestos,” “Nickel” and “Chromium” elsewhere in the Encyclopaedia). Maintenance workers are the group most likely to be at risk from these exposures.

Reduced sulphur compounds (including hydrogen sulphide, dimethyl disulphides and mercaptans) are potent eye irritants and may cause headaches and nausea in some workers. These compounds have very low odour thresholds (ppb range) in individuals not previously exposed; however, among long-time workers in the industry, odour thresholds are considerably higher. Concentrations in the range of 50 to 200 ppm produce olfactory fatigue, and subjects can no longer detect the distinctive “rotten eggs” odour. At higher concentrations, exposure will result in unconsciousness, respiratory paralysis and death. Fatalities associated with exposure to reduced sulphur compounds in confined spaces have occurred at pulp mill sites.

Cardiovascular mortality has been reported to be increased in pulp and paper workers, with some exposure-response evidence suggesting a possible link with exposure to reduced sulphur compounds (Jäppinen 1987; Jäppinen and Tola 1990). However, other causes for this increased mortality may include noise exposure and shift work, both of which have been associated with increased risk for ischaemic heart disease in other industries.

Skin problems encountered by pulp and paper mill workers include acute chemical and thermal burns and contact dermatitis (both irritant and allergic). Pulp mill workers in kraft process mills frequently experience alkali burns to the skin as a result of contact with hot pulping liquors and calcium hydroxide slurries from the recovery process. Contact dermatitis is reported more frequently among paper mill and converting workers, as many of the additives, defoaming agents, biocides, inks and glues used in paper and paper-product making are primary skin irritants and sensitizers. Dermatitis may occur from exposure to the chemicals themselves or from handling freshly treated paper or paper products.

Noise is a significant hazard throughout the pulp and paper industry. The US Department of Labor estimated that noise levels over 85 dBA were found in over 75% of plants in the paper and allied products industries, compared to 49% of plants in manufacturing in general, and that over 40% of workers were exposed regularly to noise levels over 85 dBA (US Department of Commerce 1983). Noise levels around paper machines, chippers and recovery boilers tend to be well over 90 dBA. Conversion operations also tend to generate high noise levels. Reduction in worker exposure around paper machines is usually attempted by the use of enclosed control rooms. In converting, where the operator is usually stationed next to the machine, this type of control measure is seldom used. However where converting machines have been enclosed, this has resulted in decreased exposure to both paper dust and noise.

Excessive heat exposure is encountered by paper mill workers working in paper machine areas, with temperatures of 60°C being recorded, although no studies of the effects of heat exposure in this population are available in the published scientific literature.

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Stress, the physical and/or psychological departure from a person’s stable equilibrium, can result from a large number of stressors, those stimuli that produce stress. For a good general view of stress and the most common job stressors, Levi’s discussion in this chapter of job stress theories is recommended.

In addressing the question of whether job stress can and does affect the epidemiology of cancer, we face limitations: a search of the literature located only one study on actual job stress and cancer in urban bus drivers (Michaels and Zoloth 1991) (and there are only few studies in which the question is considered more generally). We cannot accept the findings of that study, because the authors did not take into account either the effects of high density exhaust fumes or smoking. Further, one cannot carry over the findings from other diseases to cancer because the disease mechanisms are so vastly different.

Nevertheless, it is possible to describe what is known about the connections between more general life stressors and cancer, and further, one might reasonably apply those findings to the job situation. We differentiate relationships of stress to two outcomes: cancer incidence and cancer prognosis. The term incidence evidently means the occurrence of cancer. However, incidence is established either by the doctor’s clinical diagnosis or at autopsy. Since tumour growth is slow—1 to 20 years may elapse from the malignant mutation of one cell to the detection of the tumour mass—incidence studies include both initiation and growth. The second question, whether stress can affect prognosis, can be answered only in studies of cancer patients after diagnosis.

We distinguish cohort studies from case-control studies. This discussion focuses on cohort studies, where a factor of interest, in this case stress, is measured on a cohort of healthy persons, and cancer incidence or mortality is determined after a number of years. For several reasons, little emphasis is given to case-control studies, those which compare reports of stress, either current or before diagnosis, in cancer patients (cases) and persons without cancer (controls). First, one can never be sure that the control group is well-matched to the case group with respect to other factors that can influence the comparison. Secondly, cancer can and does produce physical, psychological and attitudinal changes, mostly negative, that can bias conclusions. Thirdly, these changes are known to result in an increase in the number of reports of stressful events (or of their severity) compared to reports by controls, thus leading to biased conclusions that patients experienced more, or more severe, stressful events than did controls (Watson and Pennebaker 1989).

Stress and Cancer Incidence

Most studies on stress and cancer incidence have been of the case-control sort, and we find a wild mix of results. Because, in varying degrees, these studies have failed to control contaminating factors, we don’t know which ones to trust, and they are ignored here. Among cohort studies, the number of studies showing that persons under greater stress did not experience more cancer than those under lesser stress exceeded by a large margin the number showing the reverse (Fox 1995). The results for several stressed groups are given.

1. Bereaved spouses. In a Finnish study of 95,647 widowed persons their cancer death rate differed by only 3% from the rate of an age-equivalent non-widowed population over a period of five years. A study of causes of death during the 12 years following bereavement in 4,032 widowed persons in the state of Maryland showed no more cancer deaths among the widowed than among those still married—in fact, there were slightly fewer deaths than in the married. In England and Wales, the Office of Population Censuses and Surveys showed little evidence of an increase in cancer incidence after death of a spouse, and only a slight, non-significant increase in cancer mortality.
2. Depressed mood. One study showed, but four studies did not, an excess of cancer mortality in the years following the measurement of a depressed mood (Fox 1989). This must be distinguished from hospitalizable depression, on which no well-controlled large-scale cohort studies have been done, and which clearly involves pathological depression, not applicable to the healthy working population. Even among this group of clinically depressed patients, however, most properly analysed smaller studies show no excess of cancer.
3. A group of 2,020 men, aged 35 to 55, working in an electrical products factory in Chicago, was followed for 17 years after being tested. Those whose highest score on a variety of personality scales was reported on the depressed mood scale showed a cancer death rate 2.3 times that of men whose highest score was not referable to depressed mood. The researcher’s colleague followed the surviving cohort for another three years; the cancer death rate in the whole high-depressed-mood group had dropped to 1.3 times that of the control group. A second study of 6,801 adults in Alameda County, California, showed no excess cancer mortality among those with depressed mood when followed for 17 years. In a third study of 2,501 people with depressed mood in Washington County, Maryland, non-smokers showed no excess cancer mortality over 13 years compared to non-smoking controls, but there was an excess mortality among smokers. The results for smokers were later shown to be wrong, the error arising from a contaminating factor overlooked by the researchers. A fourth study, of 8,932 women at the Kaiser-Permanente Medical Center in Walnut Creek, California showed no excess of deaths due to breast cancer over 11 to 14 years among women with depressed mood at the time of measurement. A fifth study, done on a randomized national sample of 2,586 people in the National Health and Nutrition Examination Survey in the United States, showed no excess of cancer mortality among those showing depressed mood when measured on either of two independent mood scales. The combined findings of studies on 22,351 persons made up of disparate groups weigh heavily against the contrary findings of the one study on 2,020 persons.
4. Other stressors. A study of 4,581 Hawaiian men of Japanese descent found no greater cancer incidence over a period of 10 years among those reporting high levels of stressful life events at the start of the study than those reporting lower levels. A study was carried out on 9,160 soldiers in the US Army who had been prisoners of war in the Pacific and European theatres in the Second World War and in Korea during the Korean conflict. The cancer death rate from 1946 to 1975 was either less than or no different from that found among soldiers matched by combat zone and combat activity who were not prisoners of war. In a study of 9,813 US Army personnel separated from the army during the year 1944 for “psychoneurosis”, a prima facie state of chronic stress, their cancer death rate over the period 1946 to 1969 was compared with that of a matched group not so diagnosed. The psychoneurotics’ rate was no greater than that of matched controls, and was, in fact, slightly lower, although not significantly so.
5. Lowered levels of stress. There is evidence in some studies, but not in others, that higher levels of social support and social connections are associated with less cancer risk in the future. There are so few studies on this topic and the observed differences so unconvincing that the most a prudent reviewer can reasonably do is suggest the possibility of a true relationship. We need more solid evidence than that offered by the contradictory studies that have already been carried out.

Stress and cancer prognosis

This topic is of lesser interest because so few people of working age get cancer. Nevertheless, it ought to be mentioned that while survival differences have been found in some studies with regard to reported pre-diagnosis stress, other studies have shown no differences. One should, in judging these findings, recall the parallel ones showing that not only cancer patients, but also those with other ills, report more past stressful events than well people to a substantial degree because of the psychological changes brought about by the disease itself and, further, by the knowledge that one has the disease. With respect to prognosis, several studies have shown increased survival among those with good social support as against those with less social support. Perhaps more social support produces less stress, and vice versa. As regards both incidence and prognosis, however, the extant studies are at best only suggestive (Fox 1995).

Animal studies

It might be instructive to see what effects stress has had in experiments with animals. The results among well-conducted studies are much clearer, but not decisive. It was found that stressed animals with viral tumours show faster tumour growth and die earlier than unstressed animals. But the reverse is true of non-viral tumours, that is, those produced in the laboratory by chemical carcinogens. For these, stressed animals have fewer tumours and longer survival after the start of cancer than unstressed animals (Justice 1985). In industrial nations, however, only 3 to 4% of human malignancies are viral. All the rest are due to chemical or physical stimuli—smoking, x rays, industrial chemicals, nuclear radiation (e.g., that due to radon), excessive sunlight and so on. Thus, if one were to extrapolate from the findings for animals, one would conclude that stress is beneficial both to cancer incidence and survival. For a number of reasons one should not draw such an inference (Justice 1985; Fox 1981). Results with animals can be used to generate hypotheses relating to data describing humans, but cannot be the basis for conclusions about them.

Conclusion

In view of the variety of stressors that has been examined in the literature—long-term, short-term, more severe, less severe, of many types—and the preponderance of results suggesting little or no effect on later cancer incidence, it is reasonable to suggest that the same results apply in the work situation. As for cancer prognosis, too few studies have been done to draw any conclusions, even tentative ones, about stressors. It is, however, possible that strong social support may decrease incidence a little, and perhaps increase survival.

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