Introduction
The International Agency for Research on Cancer has identified more than 200 agents as carcinogenic (Group 1) and probable carcinogens (Group 2A) to humans (
IARC, 2019). Environmental carcinogens are broadly defined as compounds that are the subset of “known” and “reasonably anticipated” human carcinogens and are considered nongenetic exogenous factors that contribute to cancer risk (
Sabo-Attwood et al., 2006;
WHO, 2011;
Wogan et al., 2004).
In Canada, neoplasms rank at the top for all-age disability-adjusted life year (DALY) counts and rates of age-standardized DALY per 100,000 (
Lang et al., 2018). A broad estimate in Ontario has identified between 3,500 and 6,500 new cancer cases each year as a result of exposure to 23 environmental carcinogens (
CCO, 2016). Some of these environmental carcinogens are present in nature and are spread across wide geographic areas, putting the entire exposed population at risk of developing cancer. However, Canada’s current cancer prevention strategies have yet to pay adequate attention to identifying and acting on the vulnerable population living in areas with potentially high environmental carcinogen exposure. Hence, health professionals have not been able to develop any environmental carcinogen-specific cancer prevention strategies in such high-risk areas. Also, local medical practitioners might not have any scope to alert local health authorities on the abnormally high prevalence of any cancer.
Newfoundland and Labrador (NL) has the highest age standardized incidence rate of cancer (587/100,000) (
CCS, 2017). Based on available environmental contamination data for NL, four environmental carcinogens were found to be present in wide geographic areas. These were arsenic and disinfection by-products in drinking water, ultraviolet rays from the sun, agricultural chemicals (herbicides/fungicides/pesticides) in ambient air, and (or) dusts affecting households living in close proximity to a golf course (
CAPE, 2016;
CBC, 2019;
de Leeuw, 2017;
GoNL, 2012;
Minnes & Kelly Vodden, 2017).
Arsenic is naturally present in underground sediments and contaminates well water (
GoNL, 2019a). The municipalities have public water systems that treat raw water before supply and regularly monitor its quality after treatment (including arsenic). Therefore, it is unlikely that there is a high arsenic level in household taps supplying public water (
Thomson et al., 2019). The communities affected by arsenic in drinking water are usually small in population size and do not have access to a public water supply and rely upon their own artesian wells, and the monitoring of water quality solely remains the responsibility of the individual well owners (
Thomson et al., 2019). Thus, there are no official reports of arsenic levels in private wells (
GoNL, 2019a).
Disinfection by-products are a very complex group of chemicals formed during the water-treatment process when disinfectants such as chlorine are added to untreated or partially treated raw water before removing organic matter (
CDC, 2016). There are more than 600 disinfection by-products in chlorinated tap water, though only two types of disinfection by-products, i.e., trihalomethanes (THMs) and haloacetic acids (HAAs) are regularly tested (
Bull et al., 2011;
CDC, 2016). THMs and HAAs have been identified as weak carcinogens (Group 2B, possible human carcinogen), and they are often used as a proxy for cancer risk assessment (
IARC, 2018;
Nieuwenhuijsen et al., 2009;
Salas et al., 2013;
WHO, 2004).
According to the Canadian Cancer Society, sunlight in Canada is strong enough to cause skin cancer, one of the most common types of cancers (
CCS, 2020). NL is known for prolonged foggy weather, and thus there is a misconception that there is a low risk of skin cancer due to a lack of direct sunlight (
CBC, 2019).
Golf courses are known for using various types of agricultural chemicals (
Golf ventures, 2019). In Canada, golf courses were exempted by municipal bylaws that restrict use of agricultural chemicals on private residential and municipal lands (
CAPE, 2016). Agricultural chemicals are heavily used on golf courses, with four to seven times greater than the recommended doses meant for any agricultural farms (
Feldman, 2020;
Golf ventures, 2019). In 2012, NL banned the use and sale of some known carcinogenic agricultural chemicals (2,4-dichlorophenoxyacetic acid, carbaryl, and 2-methyl-4-chlorophenoxyacetic acid) on lawns, but golf courses were exceptions (
Band et al., 2011;
GoNL, 2012,
2019b). Golf courses are required to provide notice to all properties located just within 15 m of the proposed agricultural chemical application sites (
GoNL, 2019b;
VoPham et al., 2015). Several studies conducted elsewhere found that populations living within 500 m of agricultural farms are subject to airborne exposure to agricultural chemicals due to drift (
Bernardi et al., 2015;
Golf ventures, 2019;
Ward et al., 2006). Agricultural chemicals are also transported via dust particles from farmlands and are carried away by strong winds. People are thus exposed to agricultural chemicals by the inhalation of contaminated air and dust. Furthermore, they are exposed to agricultural chemicals by ingestion after touching contaminated surfaces (by air and dust) in and around their residences. However, except for occupational (golfers, golf course maintenance workers) cancers, there is no published study that examined associations between residential exposure to agricultural chemicals in populations living in proximity to golf courses and a higher prevalence of the cancers caused by agricultural chemicals (
Knopper & Lean, 2004;
Kross et al., 1996;
Murphy & Haith, 2007;
Putnam et al., 2008).
We hypothesize that spatial distributions of environmental carcinogens are associated with prevalence of related cancers. The ecological study aimed to estimate the risks of cancers due to exposure to ultraviolet rays, arsenic, disinfection by-products, and agricultural chemicals.
Results
Table 2 shows that for all the environmental carcinogens, the annual prevalence rates of cancers are significantly higher in the high-risk populations. The prevalence rates of cancer among males were higher in all environmental carcinogen categories (both in high-risk and low-risk areas). There were no noticeable differences in average ages between high-risk and low-risk categories.
Since the sun’s rays become stronger as we move south, UVI also increases (
Health Canada, 2018b).
Figure 1A shows the high-risk areas only in the southern part of the province; 280,034 people (i.e., 54% of total NL population) were from high-risk areas. Estimated additional burden of cancer cases in high-risk areas were 3,043 in 10 years (2008–2017). Potential arsenic- exposed population in 10 communities was 2,876, i.e., almost 1,250 households (average household size of NL is 2.3 people) (
Statistics Canada, 2019). There are an estimated 40,000 private wells in NL that are operating without any information on their arsenic profiles (
Roche et al., 2013). If we go by the assumption that each household owns one well, our surveyed population covered only 3% of the well users. Nearly 412,000 people (79% of the total NL population) are served by the public water system, and around 15% of the serviced population are at risk of high disinfection by-products exposure (
GoNL, 2016). It is important to note that cancer prevalence rates in the communities, exposed to either high THMs or high HAAs, were not significantly higher than the low-risk population (
Table 3). It was the first evidence showing a high cancer prevalence rate in the population living near the golf course.
Discussion
To the best of our knowledge, this is the first of this kind of population-based study in Canada that has tested hypothesis of spatial associations between exposure to environmental carcinogens and a higher prevalence of cancers. The major strength of the study is its wide population coverage (both rural and urban) and understanding of spatial distributions of potentially high-risk populations. While the studies of ultraviolet rays and disinfection by-products have covered almost the length and breadth of NL, the study on agricultural chemicals has covered all the golf courses located within communities.
Despite widely available environmental monitoring data on ultraviolet rays and disinfection by-products, there are few public health strategies addressing population vulnerabilities in high-risk populations in NL. Due to existing regulatory mechanisms, regardless of efforts by a rural physician to address the arsenic contamination of private wells, there is no effective mitigation strategy in NL (
Greenham, 2018). Higher prevalence of cancers (specific to agricultural chemicals exposure) in the population living close to nine golf courses indicates significant association. There are 2,300 golf courses across Canada, and prohibition of cosmetic use of agriculture chemicals on the golf course is a contentious issue (
Golf Canada, 2015;
NGCOA). Other Canadian provinces currently do not have any provincial regulation controlling use of harmful agriculture chemicals for golf courses (CNLA). Hence, many Canadians who live close to a golf course are vulnerable to cancers and urgently need proper risk assessment.
Cancers are not attributable to a single cause, and there may be cumulative exposure to other risk factors. Therefore, to prove causal relations, future research should focus on testing biomarkers, analyzing the body burden of environmental carcinogens, examining genetic damage pertaining to specific environmental carcinogens and interviewing cancer survivors to explore other risk factors/confounders/effect modifiers relevant to particular cancers such as the duration of exposure and residence, demography, smoking, occupation, economic status, ethnicity, family history of cancer, diet and water consumption patterns, and co-exposure to other carcinogens (
Madia et al., 2019).
A well-planned strategy of combining regulation (mandatory testing of private wells, improvement of public water treatment, banning of the use of carcinogenic agricultural chemicals at golf course), health promotion (application of sunscreen before outdoor activities in summer, low-cost water filters for arsenic, and disinfection by-products and environmentally friendly turf-care), and public awareness may effectively protect the high-risk population from further exposure (
CCME, 2007;
Hirst et al., 2012;
Thomson et al., 2019).
The study has some limitations. First, the NLCCR data did not have any information on other risk factors such as smoking. Therefore, our analysis assumed that independent risk factors in both the high-risk and low-risk populations were the same. Second, the NLCCR data did not include any potential confounders/effect modifiers (mentioned above). Hence, our analysis was limited to spatial association only. We recommend the regional health authorities collect information on exposure to environmental risk factors relevant to any type of cancer while examining the patients and to incorporate the information to the existing electronic database. In this regard, proper orientation for the physicians are also needed to update knowledge on potential environmental carcinogens present in NL.