INTRODUCTION

Leukemia is a cancer that starts in stem cells of the blood. Stem cells are formed in the bone marrow (CCS 2023a). Immature blood (hematopoietic) stem cells, or blasts, normally develop into either lymphoid stem cells or myeloid stem cells. In a healthy individual, lymphoid stem cells mature into lymphocytes, which help fight infections and destroy abnormal cells, and myeloid stem cells mature into red blood cells, platelets, granulocytes, and monocytes. Red blood cells carry oxygen around the body. Platelets form clots in damaged blood vessels to stop bleeding. Granulocytes and monocytes are types of white blood cells that help fight infections. In leukemia, there is an overproduction of blast cells that develop abnormally and never become functioning blood cells. Over time, the blast cells crowd out normal blood cells so that they can’t do their jobs.

In Canada, leukemia is diagnosed at a rate of 15 cases per 100,000 persons and accounts for about 3% of all new primary cancers. It is estimated that in 2022, 6,700 Canadians will be diagnosed with leukemia and 3,100 Canadians will die from leukemia (CCS 2023a). There are many different types of leukemia (CCS 2023b). In adults, chronic lymphocytic leukemia (CLL) and acute myeloid leukemia (AML) are the most common leukemias. CLL accounts for about one-quarter of the new cases of leukemia and mainly affects older adults.

Leukemia was the first medically observed human cancer related to ionizing radiation in the follow-up study of atomic bomb survivors. Myeloid leukemia and acute lymphocytic leukemia (ALL) were linked to external radiation in Japanese atomic bomb survivor studies (Preston et al. 1994; Pierce and Preston 2000). A meta-analysis of 23 studies confirmed that, excluding CLL, protracted exposure to low-dose gamma radiation is significantly associated with leukemia, and the preferred estimate of leukemia risk at 100 mGy was 0.19 (95% CI 0.07 to 0.32) (Daniels and Schubauer-Berigan 2011).

Underground uranium miners are chronically exposed to low levels of radon (222Rn) and its progeny along with γ-radiation. While risks of leukemia from acute and high doses of γ-radiation are well characterized, risks from lower doses and dose-rates from radon exposure are controversial. A study in the Eldorado uranium workers cohort of Canada (Zablotska et al. 2014) found no statistically significant association between radon exposure or γ-ray doses, or a combination of both, and mortality or incidence of any hematologic cancer. A study of leukemia in German miners (Möhner et al. 2006) did suggest an elevated risk of leukemia for cumulative radon progeny exposures of ≥400 working level months (WLM). Another study in the Pribram region of the Czech Republic investigated incidence of leukemia, lymphoma, and multiple myeloma among a subcohort of 2,393 uranium miners (Rericha et al. 2006), where an elevated risk for all leukaemia combined (risk ratio (RR) = 1.75, 95%CI 1.10 to 2.78) and for CLL (RR = 1.98, 95%CI 1.10 to 3.59) was observed when comparing high radon exposure to low radon exposure. Suggestive associations between myeloid leukaemia and Hodgkin’s lymphoma (HL) with radon exposure were reported. With the same cohort, a followup study (Kelly-Reif et al. 2019) found elevated risks for all leukaemia, HL, multiple myeloma, myeloid leukemia, and lymphoid leukemia.

Several ecologic studies (Laurier et al. 2001) reported an association between indoor radon exposure and leukemia. The results of the published ecological studies appear relatively concordant and suggest the existence of an association between radon concentration and leukemia risk at a geographic level. The purpose of this study was to examine the correlations between residential radon levels and the incidence rates of various subtypes of leukemia in different provinces of Canada.

DATA SOURCES AND METHODS

Canada has 10 provinces and three territories. The three territories (the Northwest Territories, the Yukon, and Nunavut) are primarily North of 60° latitude. While they account for 40% of Canada’s land mass, they represent only approximately 0.3% of the Canadian population. Because of the relative rareness of the disease and very low population in the three territories, incidence rates of leukemia are often not available or suppressed to meet the confidentiality requirements of the Statistics Act. Therefore, this study analyses available data only for the 10 Canadian provinces.

Indoor radon concentration

With the lowering of the Canadian indoor radon (222Rn) guideline from 800 to 200 Bq m−3 in June 2007, there has been a wave of long-term radon testing in residential homes. Based on those community and nationwide surveys, radon distribution characteristics were re-assessed for 10 provinces in Canada (Chen 2021). In the re-assessmnet, only long-term radon measurements with alpha track detectors were considered. Thoron (220Rn) is an isotope of radon. Detectors sensitive to thoron can impact the results of radon (222Rn) measurement. The alpha track detectors used in Canadian surveys conducted by various levels of government and included in the re-assessment (Chen 2021) are less than 2% sensitive to thoron (220Rn) compared to their sensitivity to radon (222Rn) (Chen and Moir 2012). The summary results of indoor radon (222Rn) concentrations in units of Bq m−3 are listed in Table 1.

Table 1 - Indoor radon distribution characteristics [geometric mean (GM) and geometric standard deviation (GSD)] by province. Province Population in 2006 Number of homes tested GM
(Bq m−3) GSD Newfoundland and Labrador (NL) 505,469 810 41 2.91 Prince Edward Island (PEI) 135,851 113 24 2.94 Nova Scotia (NS) 913,462 759 55 3.49 New Brunswick (NB) 729,997 1,086 73 3.36 Quebec (QC) 7,631,552 2,780 47 2.72 Ontario (ON) 12,665,346 5,458 45 2.50 Manitoba (MB) 1,148,401 1,400 124 2.44 Saskatchewan (SK) 968,157 1,406 114 2.21 Alberta (AB) 3,290,350 3,709 93 1.77 British Columbia (BC) 4,113,487 3,809 33 2.06
Leukemia incidence rate

Statistics Canada maintains the Canadian Cancer Registry (CCR), which is comprised of data supplied annually by the provinces and territories of Canada. For various subtypes of leukemia, the number of new cancer cases, age standardized incidence rates per 100,000 population with 95% confidence intervals, and average age at diagnosis are publicly available on the website of Statistics Canada (2022) for the period from 1992 to 2019. The subtypes of leukemia are listed in Table 2.

Table 2 - Types of leukemia (Statistics Canada 2022) based on the World Health Organization International Classification of Diseases for Oncology (WHO 2013). Primary cancer Topography code and morphology code in ICD-O 3rd Edition Hodgkin lymphoma (HL) 9650-9667 Non-Hodgkin lymphoma (NHL) 9590 to 9597, 9670 to 9729, 9735 to 9738; 9811 to 9818, all sites except C42.0, C42.1, C42.4; 9823, all sites except C42.0, C42.1, C42.4; 9827, all sites except C42.0, C42.1, C42.4; 9837, all sites except C42.0, C42.1, C42.4 Myeloma 9731, 9732, 9734 Acute lymphocytic leukemia (ALL) 9826, 9835-9836; C42.0, 9811-9818, 9837; C42.1, 9811-9818, 9837; C42.4, 9811-9818, 9837 Chronic lymphocytic leukemia (CLL) C42.0, 9823; C42.1, 9823; C42.4, 9823 Acute myeloid leukemia (AML) 9840,9861,9865,9866,9867,9869,9871-9874,9895-9897,9898,9910,9911,9920 Chronic myeloid leukemia (CML) 9863, 9875, 9876, 9945, 9946 Other leukemia (OL) 9733, 9742, 9800, 9801, 9805 to 9809, 9820, 9831, 9832 to 9834, 9860, 9870, 9891, 9930, 9931, 9940, 9948, 9963, 9964; C42.0, 9827; C42.1, 9827; C42.4, 9827

To limit the potential residual disclosure, in line with CCR reporting requirements, incidence counts have to be randomly rounded either up or down to a multiple of 5. The random rounding rounds all non-zero cell counts (those that are not evenly divisible by 5) to the adjacent lower or higher multiple of 5. By design, differences between the rounded counts and actual counts should never exceed 4, and a count was more likely to be rounded to the nearest multiple of 5. For provinces having rather small populations such as PEI, NL, and NB, number of new leukemia cases can be very low. Therefore, randomly rounded counts lower than 10 (i.e., rounded counts of 0 or 5) have large uncertainty and should be used with caution. Age-standardized incidence rates (ASIRs) were derived from dividing the random-rounded counts by the population.

Analysis method

Simple linear fitting (ANOVA linear regression) was applied for age-standardized incidence rates per 100,000 population as a function of population-weighted geometric mean radon concentration in provinces of Canada. The analyses were conducted for all subtypes of leukemia and lymphoma: HL, NHL, Myeloma, ALL, CLL, AML, CML, and Other leukemia.

RESULTS

In this study, 10-y averaged age-standardized incidence rates (ASIR) per 100,000 persons were calculated by leukemia subtype and for each province in Canada in order to further reduce statistical variation/uncertainty. The province of Quebec, the second largest province in Canada, has no data available for 2010 onward. In order to include data from the province of Quebec, a 10-y period from 2000 to 2009 was selected. Table 3 summarizes 10-y averaged ASIRs with 95% confidence intervals, number of new cases per year, and average age at diagnosis for each subtype of leukemia in Canada. The incidence rates are highest for NHL followed by Myeloma, CLL, and AML. The incidence rates are low for HL and OL and very low for CML and ALL. For all subtypes of leukemia, incidence rates are higher in males than females. ALL is more common in younger adults, while most other subtypes are common for adults between 60 to 70 y of age.

Table 3 - Ten-year (2000-2009) averaged statistics of various subtypes of leukemia in Canada. Canada HL NHL Myeloma ALL CLL AML CML OL Average age at diagnosis 41.6 64.5 70.4 24.8 71 62 64.4 65.1 Number of new cases 890 6,145 1,918 368 1,898 1,018 474 644 ASIR (95% CI)
(both sexes) 2.81(2.62, 2.99) 20.8
(20.3, 21.3) 6.61
(6.30, 6.91) 1.11
(1.01, 1.25) 6.52
(6.23, 6.82) 3.40
(3.20, 3.60) 1.59
(1.44, 1.74) 2.19
(2.02, 2.35) ASIR (95% CI)
(males) 3.14
(2.87, 3.44) 24.6
(23.7, 25.4) 8.19
(7.67, 8.69) 1.30
(1.12, 1.48) 8.89
(8.36, 9.40) 4.07
(3.75, 4.44) 2.06
(1.81, 2.33) 2.85
(2.54, 3.15) ASIR (95% CI)
(females) 2.45
(2.22, 2.71) 17.7
(17.0, 18.4) 5.40
(5.02, 5.75) 0.99
(0.80, 1.10) 4.68
(4.35, 5.01) 2.89
(2.61, 3.15) 1.26
(1.08, 1.41) 1.66
(1.46, 1.86)

Ten-year averaged ASIRs per 100,000 population for eight subtypes of leukemia for both males and females were calculated for each province in Canada, as summarized in Table 4. When broken down by province, even for both sexes combined, most subtypes of leukemia have low or very low incidence rates, with wide 95% confidence intervals, especially for provinces with low populations.

Table 4 - Ten-year averaged ASIRs per 100,000 population for different subtypes of leukemia by province for both sexes. Province HL NHL Myeloma ALL CLL AML CML OL NL 1.96a (0.96, 3.75) 17.4 (13.7, 21.0) 4.29 (2.67, 6.66) 0.74a (0.30, 1.58) 2.73a (1.65, 4.51) 2.34a (1.24, 4.23) 1.11a (0.44, 2.43) 1.74a (0.79, 3.49) PEI 2.24a (0.74, 5.48) 20.1 (13.2, 29.5) 7.69a (3.73, 14.4) x 6.96a (3.41, 12.9) 4.15a (1.78, 8.50) 1.58a (0.51, 3.76) 0.83a (0.28, 2.08) NS 3.02 (2.00, 4.38) 21.8 (18.8, 24.8) 6.23 (4.64, 7.88) 1.09a (0.51, 2.02) 5.98 (4.45, 7.69) 3.34 (2.29, 4.75) 1.73 (0.99, 2.83) 2.35 (1.48, 3.59) NB 2.64 (1.63, 4.14) 22.8 (19.3, 26.3) 6.85 (4.99, 8.93) 1.29a (0.60, 2.44) 5.78 (4.16, 7.81) 2.99 (1.87, 4.57) 1.61a (0.84, 2.85) 1.79a (0.99, 3.12) QC 3.01 (2.62, 3.40) 20.4 (19.3, 21.4) 6.95 (6.33, 7.54) 1.30 (1.04, 1.56) 6.07 (5.49, 6.66) 3.22 (2.81, 3.64) 1.59 (1.28, 1.85) 2.38 (1.99, 2.72) ON 2.85 (2.54, 3.16) 20.8 (19.9, 21.6) 6.90 (6.41, 7.39) 0.93 (0.76, 1.09) 6.08 (5.62, 6.56) 3.59 (3.22, 3.94) 1.50 (1.27, 1.73) 2.54 (2.24, 2.83) MB 2.67 (1.80, 3.86) 22.8 (20.0, 25.7) 6.33 (4.83, 7.84) 1.30a (0.73, 2.14) 9.36 (7.51, 11.2) 3.16 (2.19, 4.43) 1.69 (1.03, 2.71) 1.72 (1.05, 2.74) SK 3.04 (2.06, 4.43) 21.3 (18.4, 24.3) 6.22 (4.62, 782) 1.27a (0.71, 2.24) 9.30 (7.36, 11.3) 3.50 (2.43, 4.96) 1.61 (0.91, 2.68) 2.28 (1.44, 3.49) AB 2.73 (2.14, 3.32) 20.6 (18.8, 22.4) 6.63 (5.61, 7.67) 1.29 (0.92, 1.74) 9.01 (7.80, 10.2) 3.53 (2.79, 4.26) 1.81 (1.32, 2.38) 1.39 (0.97, 1.98) BC 2.48 (2.01, 2.96) 21.0 (19.6, 22.4) 5.68 (4.92, 6.42) 1.26 (0.93, 1.62) 6.56 (5.76, 7.36) 3.30 (2.74, 3.87) 1.77 (1.36, 2.16) 1.57 (1.17, 1.97)

For the province of Newfoundland and Labrador (NL), results for six out of eight subtypes of leukemia must be used with caution due to large uncertainties, because in one or more years from 2000 to 2009, there were either no data or data being suppressed to rounded zero or 5 to meet the confidentiality requirements of the Statistics Act. These subtypes are HL, ALL, CLL, AML, CML, and OL marked with a “*” in Table 4.

For the smallest province, Prince Edward Island (PEI), with a population of 135,851 in 2016, the ASIRs of ALL were either completely unavailable or rounded to zero from 2000 to 2009. The 10-year averaged ASIRs of other subtypes of leukemia should be used with caution, except for NHL.

ALL has the lowest incidence rate in Canada, about one case per 100,000 persons as shown in Table 3. The 10-y averaged ASIRs of ALL should be used with caution for the provinces of NL, NS, NB, MB, and SK due to very low numbers of new cancer cases and large uncertainties being introduced after randomly rounding to zero or 5.

The impact of residential radon exposure on the leukemia incidence rates was examined with linear regression using geometric mean (GM) values given in Table 1 and ASIRs in Table 4. The analysis was conducted first with all available data and then excluding those ASIRs derived from rounded counts of 0 and 5 due to large uncertainties, as marked to be used with caution in Table 4. Results of ANOVA linear regression analysis (for R2 > 0.2) are summarized in Table 5.

Table 5 - Results of linear fitting (R2) and ANOVA linear regression (for R2 > 0.2) between subtypes of lekemia and geometric mean radon concentrations. Leukemia All available data included Excluding data with large uncertainties Subtype R 2 ANOVA linear regression R 2 ANOVA linear regression HL 0.1837 0.0069 NHL 0.2781 F 1,9 = 3.082, p = 0.1172 0.2781 F 1,9 = 3.082, p = 0.1172 Myeloma 1.0E-07 0.0717 ALL 0.2587 F 1,8 = 2.443, p = 0.1620 0.0758 CLL 0.5304 F 1,9 = 9.035, p = 0.0169 0.7677 F 1,7 = 19.83, p = 0.0043 AML 0.0056 0.0004 CML 0.1028 0.0149 OL 0.0243 0.0800

The analyses with all available data including data with large uncertainties (i.e., randomly rounded counts of 0’s and 5’s) found slightly positive but not statistically significant association between indoor radon level and subtypes of NHL and ALL, as shown in Fig. 1. It can be seen clearly that uncertainties are larger for provinces with lower populations. While there were no data with large uncertainties for NHL in all provinces from 2000 to 2009, six out of 10 provinces have data with large uncertainties for ALL as marked in Table 4, mainly due to the rareness of ALL cases. Therefore, the relative significance of the positive correlation between average indoor radon concentration and ALL incidence rate is much weaker and with very large uncertainty. When excluding ASIRs derived from data with large uncertainties, there is no correlation between average indoor radon concentration and ALL incidence rate (R2 = 0.0758).

Fig. 1:

Ten-year averaged ASIRs per 100,000 population for NHL (a) and ALL (b) as a function of geometric mean radon concentration in the provinces of Canada.

The association between average indoor radon concentration and CLL incidence rate is statistically significant (p = 0.0167), as shown in the upper panel of Fig. 2. When excluding ASIRs derived from provinces with large counting uncertainties (i.e., excluding data from NL and PEI), the association between average indoor radon concentration and CLL incidence rate improved significantly (p = 0.0042), as shown in lower panel of Fig. 2.

Fig. 2:

Ten-year averaged age-standardized CLL incidence rate per 100,000 population as a function of geometric mean radon concentration in the provinces of Canada.

In Canada, the incidence rates of NHL are highest among all subtypes of leukemia. With relatively higher incidence rates, an analysis was conducted for males and females separately. The results are presented in Fig. 3. The incidence rates are much higher in males than in females for all provinces. There is no correlation between average indoor radon concentration and NHL incidence rate for males (upper panel of Fig. 3). For females, the correlation between average indoor radon concentration and NHL incidence rate is statistically significant with p = 0.0121 (lower panel of Fig. 3).

Fig. 3:

Ten-year averaged age-standardized NHL incidence rate per 100,000 population as a function of geometric mean radon concentration for males and females in the provinces of Canada.

In Canada, the incidence rates of CLL are statistically significantly correlated with average indoor radon levels. Further analysis by sex showed that while the CLL incidence rates are higher in males, the correlation with average indoor radon concentration is slightly stronger for females, as demonstrated in Fig. 4.

Fig. 4:

Ten-year averaged age-standardized CLL incidence rate per 100,000 population as a function of geometric mean radon concentration for males and females in the provinces of Canada (excluding NL and PEI).

DISCUSSION AND CONCLUSION

Based on the solubility of 222Rn in blood, the calculated annual radiation dose to cells in bone from continuous inhalation of 222Rn at a concentration of 100 Bq m−3 was 0.0016 and 0.0018 mGy for males and females, respectively (Harley and Leslie 2023). For 1 y of exposure to radon concentration of about 22 Bq m−3, the committed effective dose to red bone marrow was estimated to be 80 μSv (Kendall et al. 2009). In view of the generally low doses to the bone marrow arising from exposure to radon in dwellings, it is unlikely that risks of the order predicted from current radiation risk estimates for leukemia could have been observed, as indicated in the UNSCEAR 2006 Report (UNSCEAR 2008).

While several studies did not support exposure to residential and/or occupational radon as a causal factor in leukemia (Lubin et al. 1998; Steinbuch et al. 1999; Law et al. 2000; UNSCEAR 2008; Zablotska et al. 2014; Navaranjan et al. 2016), some studies observed suggestive and positive association between radon exposure and incidence rate of certain subtypes of leukemia (Laurier et al. 2001; Evrard et al. 2005; Möhner et al. 2006; Rericha et al. 2006; Kelly-Reif et al. 2019).

In Canada, Henshaw et al. (1990) reported a significant correlation between the incidence of AML and average indoor radon concentrations in the provinces, while a later study by Miller et al. (1993) observed no statistically significant correlations for any age/sex groups examined at the city level. These two early studies used radon data from the cross-Canada radon survey carried out in the late 1970s, where radon concentrations in homes in 19 cities were characterized with a single “grab sample” collected on a summer day (McGregor et al. 1980). In this study, average radon concentrations at a provincial level were determined from long-term (3 mo and more) radon measurements in a total of 21,330 homes in various communities and health regions (Chen 2021). With more accurate radon distribution characteristics, the analysis using all available data in 10 provinces found slightly positive but not statistically significant association between indoor radon exposure and ALL, where the uncertainties are large due to rareness of the disease. The analysis showed that the incidence rate of NHL is statistically significantly correlated with average indoor radon concentration for Canadian females (p = 0.01210) but not for males. At the provincial level, the association between indoor radon exposure and CLL is statistically significant (p = 0.0167), and the correlation is somewhat stronger for females. No correlation with indoor radon level was found for AML and any other subtypes of leukemia evaluated in this study.

Acknowledgments

The author thanks Naomi Harley for her encouragement to conduct this study.

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