Assessing
cancer mortality in high natural background radiation areas: a systematic review
Seyyed Mohammad Taghi Razavi-Toosi
1,2, Morteza Bakshi 2, Rohullah
Yousefi 2*
1 Medical
Biotechnology Research Center, School of Paramedicine, Guilan
University of Medical Sciences, Rasht, Iran
2 Student
Research Committee, School of Paramedicine, Guilan
University of Medical Sciences, Rasht, Iran
Corresponding Authors: Rohullah
Yousefi
* Email: Rohan.kingb32@gmail.com
Abstract
Introduction: Low background radiation levels are constantly around us, but
generally there are some high natural background radiation areas (HNBRAs) in
the world including Ramsar in Iran, Guarapari in
Brazil, Kerala in India, Arkaroola in Australia, and Yangjiang
in China. The present study aims to explore the relationship between living in
HNBRAs and cancer mortality rate.
Materials and Methods: A perfect search was
conducted in Google Scholar, Scopus, PubMed, and databases and articles with
the key terms "High natural background radiation", "cancer
prevalence in HNBRAs", " natural radiation" and " mortality"
using MeSH.
Results: The results of this study are based on articles published in national
and international journals, dissertations, and reference sites. In a total of
156 documents, 33 (21.15%) were selected. Many epidemiological and experimental studies demonstrated that at low
natural background radiation doses, cancer incidence is not proportionally
related to living in HNBRAs, while even beneficial effects are often observed
at low natural background radiation doses. It is evident that chronic radiation
exposure is not only less harmful per unit dose than acute radiation but can
also induce cellular responses such that adaptation phenomena appear. Thus,
some researchers have reported a direct relationship between HNBR and cancer
mortality, and some others have found no relationship between the two variables.
Conclusion: More recent studies have highlighted the absence of any direct
connection between high natural background radiation and the prevalence of
cancer in people living in HNBRAs. Some studies have suggested that low natural
background radiation is not only harmless but may be beneficial to health
through adaptations, while others believe that even the smallest doses of
radiation are harmful.
Keywords: Cancer, Natural radiation, High natural background radiation areas,
Ramsar, Mortality
Introduction
Radiation
refers to the release or transfer of energy in the form of waves or particles
that can penetrate matter and humans. Radiations are divided into two groups of
ionizing and non-ionizing rays according to their effects on matter (1). Radioactive materials exist
throughout nature and can be detected in soil, rock, water, air, and plants (2). These materials enter the body by
inhalation or swallowing (1). In addition to exposure from
inside the body, humans are also externally affected by radioactive materials
outside the body and space (cosmic radiation) (3). The average natural radiation rate
is about 2.4 Millie Sievert (mSv) per year (4). This amount is four times the
global average rate of artificial radioactivity, which was about 0.6 mSv per
year in 2008 (2). In some rich countries, the frequent use of medical imaging leads
to higher average rates of artificial radioactivity compared to the natural
radioactivity rate (5). In Europe, natural radioactivity
ranges from 2 mSv per year in England to more than 7 mSv per year for some
groups in Finland (6) some areas contain doses or amounts
higher than the national average. In general, places with high natural
background radiation include Ramsar in Iran, Guarapari
in Brazil, Kerala in India, Arkaroola in Australia, and Yangjiang
in China (5, 7). The problem of high background
radiation in the world has been attracting the attention of researchers for a
long time (8). The history of radiobiology shows
that the biological effect of relatively high radiation doses was recognized
only shortly after the discovery of X-rays and radioactivity, but the effects
of low radiation doses on human health are still unknown and are the focus of
many investigations (9). There is controversy over whether
low radiation rates pose a significant health risk. On one hand, the linear
no-threshold model (LNT) assumes that even the smallest amounts of radiation
are harmful (10) and, on the other hand, it argues
that exposure to low-level radiation is not only harmless (11), but may also benefit health
through adaptation (12-15).
According
to the United Nations Scientific Committee on the Effects of Atomic Radiation
(UNSCEAR, 2000), the coastal city of Ramsar has the highest level of background
radiation among all residential areas in the world (16). For example, the average natural
radiation rate is about 13 mSv per year in Kerala and about 240 mSv per year in
Ramsar (17). The use of laboratory animals in
medical sciences has led to progress in the prevention and treatment of
diseases so that they are used to study many incurable human diseases such as
heart failure and stroke (18, 19). Hence, high natural background
radiation in Ramsar has motivated researchers to conduct many experiments on
the effects of these radiations on vital parameters in animal and human samples
(20, 21). Surprisingly, the maximum annual
dose allowed for radiation technologists (radiographers) is 20 mSv per year,
and following the recommendation of the International Commission on
Radiological Protection (ICRP), to prevent the possible effects of radiation
such as cancer and genetic diseases, the annual dose for ordinary people should
be less than 1 mSv (22). A comparison of natural background
radiation doses in different regions of the world shows the radiation rate in
Ramsar is about 90 times the dose that forced the evacuation of 200,000
residents in the areas contaminated by the Chernobyl disaster in 1986 (23). Simple scientific estimates have
shown more physical and health problems in all residents of high natural
background radiation areas (HNBRAs) in Ramsar with radiation exposure of a
maximum of 240 mSv per year compared to normal people with an average radiation
rate of 1 mSv per year (24-26). However,
previous studies in the literature have reported inconsistent results (27). To this end, the present study
aimed to investigate the cancer mortality rate in people living in high natural
background radiation areas (HNBRAs) and to find out whether there is a
relationship between living in these areas and cancer deaths.
Materials and Methods
One of the inclusion criteria for entering the research was a
quantitative study mentioning the mortality rate due to cancer in HNBRAs. The
exclusion criteria of this research were: not mentioning the mortality rate
caused by cancer in HNBRAs, lack of relation between the study and the research
topic, qualitative articles, and articles with repetitive topics.
A perfect search was conducted using the Persian keywords and
English synonymous in international databases including MEDLINE, Google
Scholar, Scopus, PubMed, and databases and articles with the key terms
"High natural background radiation", "The
mortality rate due to cancer in high natural background radiation areas",
"natural radiation" and "mortality" using MeSH and Boolean operators such as "AND",
"OR" and "NO" were searched published by 11/30/2022 and a
number of articles related to prevalence of cancer in residents of high natural
background radiation areas were selected. The search databases were to
accomplish searches with high sensitivity (Highly Sensitive Searching) and also
the search was achieved by a senior researcher and expert in the field of
searching databases. The entire process of research including, search,
selection of contents, typicality valuation of studies, and data gathering was
accomplished independently by two researchers to evade publication bias, and
the third researcher was performing the final assessment in the event of a
conflict. After the search, EndNote𝑇𝑀 software was
used to reveal duplicates. Also, manual searching was done by reviewing the
reference list of suitable articles.
Results
In a
systematic comprehensive search, 156 articles relevant were found on the
above-mentioned database published by 11/30/2022. After the checking Items
found, 62 of them were eliminated via investigating titles and their abstracts
and 94 were eligible for evaluation of their full-text.
Afterward,
articles that lacked inclusion criteria or studies that had incomplete
information or had exclusion criteria were excluded from this research.
Eventually, 28 (21.15%) remaining documents were selected in this systematic
review. The characteristics of a number of studies used in the present study
are given in Table 1.
Table 1. The characteristics of the studies
included in the present study.
|
Name |
Year |
Location |
Result |
|
BEIR VII (1,2) |
1990, 2006 |
Generally |
The number of radiation-initiated
cancers is exceptionally little compared with the number of actually happening
cancers making location of this overabundance exceptionally troublesome. |
|
Gianferrart et al. (29) |
1962 |
Piemonte, Italy |
Mortality rates from other causes as well as cancer are higher in
HBR than in NBR. |
|
Mortazavi et
al. (30) |
2005 |
Ramsar, Iran |
Appeared that the frequency of
lung cancer in individuals living in Ramsar is lower than within the control
bunch. Also lymphocytes
experienced a compromise, and their reaction to rehashed high-dose radiation
was lower. |
|
David Elroei
et al. (31) |
2021 |
United States |
Appeared a critical diminishment within the mortality rate from
cancers in both men and women. |
|
Hendry et al.
(32) |
2009 |
Guarapari, Brazil;
Kerala, India; Ramsar, Iran; Yangjiang, China |
These considers illustrated no
expanded dangers within the HNBR ranges compared to control/reference
populaces. The later ponder in Yangjiang, China,
appeared a noteworthy abundance of non-cancer mortality. In Iran, as it were
chromatid-type variations (not particular for radiation) were found to be
enhanced. |
|
Yamaoka et al. (33) |
2004 |
Okayama, Japan |
The result shows us that the small dose of radon has healing
effects and can be used as a treatment. |
|
Thompson et
al. (34) |
2008 |
Case - Control Study |
In their studies, they found a
link between lung cancer and radon exposure. |
|
Fornalski et al. (35) |
2011 |
Poland |
The results indicate that in different doses, the relation can be
seen as increasing, decreasing and hormesis effects. |
|
Denton et al.
(36) |
2013 |
Guam, USA |
Data shows that residents of areas
with higher radon levels are more resistant to lung cancer than their
counterparts. |
|
Wei et al. (37) |
2000 |
Yangjiang, China |
The results of the human body's adaptive response test show that
long-term exposure to high background radiation causes lymphocytes to show
less sensitivity in laboratory conditions. |
|
Hauri et al. (38) |
2013 |
Switzerland |
The gotten comes about did not
appear a relationship between indoor radon and children's cancer. There was
no prove of direct exposure–response affiliations for any of the results. |
|
Jaikrishan et al. (39) |
2013 |
Kerala, India |
Appeared no coordinate relationship between radiation levels in
HNBRs and cancer mortality. Moreover, did not influence stillbirths and major
intrinsic mutations in newborn children. |
|
Kumar et al. (40) |
2012 |
Kerala, India |
The DNA harm of those who lived
within the HNBR region diminished with age, whereas the DNA harm of the
reference bunch expanded with age. |
Discussion
There is no place on the earth without natural ionizing background
radiation. This background radiation is now much lower than when our planet was
formed. This clearly shows that organisms living in the same environment for a
long time evolve to adapt to this radiation dose (41). Many studies conducted in this
field have not shown that background radiation has caused an acute or latent
disease such as cancer (41). Numerous epidemiological and
experimental studies demonstrated that at low natural background radiation
doses, cancer incidence is not proportionally related to living in HNBRAs,
while even beneficial effects are often observed at low natural background
radiation doses (42). Moreover, it is evident that
chronic radiation exposure is not only less harmful per unit dose than acute
radiation but can also induce cellular responses leading to adaptation
phenomena (43-45).
A review study by Aliyu and Ramli on studies addressing life in
HNBR areas has critically received extensive attention (45). The authors concluded that the
number of epidemiological studies may not be sufficient to rule out the effect
of increased radiation in HNBRAs. For instance, cytogenic studies on biological
systems have shown some chromosomal aberrations in people living in HNBRAs (46). However, most of the reviewed
studies have not found any relationship between cancer mortality and reduced
life expectancy. Moreover, Mortazavi et al, showed that the incidence of lung
cancer in people living in Ramsar is lower than in the control group (30). Interestingly, Ghiassi-Nejad et
al, found the presence of an adaptation response in people living in HNBRAs (47).
As stated earlier, existing regulations on radiation protection
rely heavily on the LNT model, which predicts that any dose of ionizing
radiation, however small, carries a certain risk of harm to health,
particularly cancer (48). This hypothesis has its origin in
the wrong behavior of several influential scientists in the world (49).
The data presented by Gianferrart et al,
on cancer mortality in HNBRAs and natural background radiation areas (NBRAs)
show that mortality is related to the difference in internal and external
radiation and the effects of radiation are more obvious due to increased
cumulative dose at the age of 61 to 80 years (29).
It is not reasonable to confirm the relationship between cancer
incidence and natural radiation based on the results reported by Gianferrart et al (29). However, some studies have shown
that natural sources of small doses of radiation can increase the probability
of developing cancer (50).. In contrast, Elroei
et al, showed a significant reduction in the mortality rate from lung and
bronchial, pancreatic, colon, and rectal cancers in both men and women living in HNBRAs and were stated that can even have
useful health effects in humans (31).
According to the study by Gianferrart et
al, significant reductions were observed for brain cancer and bladder cancer
only in men. Besides, there is a clear tendency for liver and bile duct cancer (29). In contrast, no significant
effects were observed for leukemia, kidney, pelvic, and stomach cancers nor
gender-specific cancers (cervical, ovarian, breast, and prostate) for either
men or women (29).
Natural background radiation levels on the earth vary
significantly, even by a factor of two. The magnitude of the radiation level
varies from place to place with a global average annual effective dose of about
2.5 mS (32). Jagger showed that in NBR areas,
the radiation rates at lower altitudes are lower than at higher altitudes (13). Besides, a comparison of low and
high areas in terms of cancer rates showed lower cancer rates in high altitudes
(51).
However, in some places (e.g., Ramsar in Iran), the radiation
levels increase several times (30, 32, 45). Thus, areas
with dose rates higher than about 10 mSv per year are commonly called HNBRAs (30, 32, 45). The results
obtained so far are still speculative and it is not possible to say how big the
uncertainties are, nor is it clear whether the observed chromosomal aberrations
are correlated with cancer incidence and/or mortality (41). This article further emphasized
the relationship between dose level, dose rate, and cancer mortality in groups
of individuals living in HNBRAs (46). Moreover, since most of the
previous studies emphasized a linear relationship, ellipse analysis was
performed in this study to investigate this relationship (31).
Hendry et al, reviewed the results of HNBR radiation studies and
the cancer risk of populations living in HNBRAs (Guarapari
in Brazil, Kerala in India, Ramsar in Iran, and Yangjiang
in China) to estimate the potential health risks at low doses (32). It is worth noting that low doses
of radon can even have healing effects, as discussed by Yamaoka et al (33). As no statistically significant
evidence of harmful effects of doses has been observed, a review of
case-control studies indicated no clear association between high-level radon
exposure and lung cancer in miners (30).
Hendry et al, have provided convincing evidence of the relationship
between long-term exposure to radiation and the occurrence of disease in a
certain dose range (32). Moreover, they have reasonably
argued that "many countries that have HNBRAs lack health statistics,
especially cancer prevalence statistics (32). An analysis of 28 reports on lung
cancer, possibly caused by radon , shows that the published data have large
gaps and are scattered (52). For instance, there are no clear
findings for a radon concentration of 800 Bq/m3
(Becquerel per cubic meter) (52). These statistical findings of
radon contradict the conclusions drawn by UNSCEAR highlighting the high
radiation risk, even at a radon concentration of 100 Bq/m3
(53). Ecological studies have been often
performed on large and widely reported cohorts, and our knowledge of the health
effects of ionizing radiation is largely based on such studies(54). For example, Cohen’s controversial
analysis of the risk of radon shows a reduction in lung cancer (55). The incidence of cancer with
increasing radon exposure was later confirmed in case-control studies by
Thompson et al (34). Additional ecological studies have
analyzed the risk of cancer caused by natural radiation in China (Wei et al) ,
Guam (Denton et.al) , Poland (Fornalski et al) (35), the United States and Switzerland
(Hauri et al) (35-38). Another
recent case-control study conducted by Jaikrishan et
al in 2013 (39) did not show a direct relationship
between radiation levels in HNBRs and cancer mortality. Moreover, HNBR
radiation levels in Kerala, India, did not affect stillbirths and major
congenital malformations in infants (56).
The often-stated adaptation theory assumes that people living in
HNBRAs have adapted to the radiation levels in the area (44). Previous increases in natural
radiation levels, assuming to be correct, indicate that radiation protection
recommendations can consider the radiation level in a given environment as the
best reference level (32, 45). Feinendegen
et al and Scott et al, have focused on mechanisms that are not yet fully
understood and do not involve adaptive protection as far as regulators of
radiation protection are concerned (52, 57). On the other hand, Mortazavi et
al, showed that lymphocytes from individuals residing in the HNBR area of
Ramsar underwent a compromise, and their response to repeated high-dose
radiation was lower (30). The results of another study
conducted by Kumar et al, in the HNBR area of Kerala, India, showed that the
incidence of DNA damage per person decreased with age, while in the control
population, the incidence of DNA damage, as expected, increased with age (40). Finally, the lack of any
correlation between living in HNBRs and cancer deaths in biophysical studies
can be attributed only to this adaptive protection (adaptive response effect) (52, 57), as a general basis for radiation
hormesis. The elliptic analysis is more effective than linear analysis in
describing the data with functions containing several different components (58).
Conclusions
Cancer mortality risks from low
doses, like high background radiation exposures, appear to be absent or much
lower than effects commonly assumed, especially when assessed by
epidemiological methods alone. However, the current epidemiological and
experimental data do not favor low-induced doses. Following the findings of the
present study, the claim that exposure to HNBR rates leads to cancer is
unjustified and misleading. The results of the Bayesian analysis, as presented
in this paper and applied to the available data for HNBR regions, indicated
that cancer mortality decreases in proportion to dose. However, these results
could not lead to any positive correlation between cancer mortality and
radiation doses. Therefore, if hormesis, i.e. benefits
outweighing harm, is not proven, it can still be argued that there must be a
minimum threshold dose for cancer, where benefits and harms balance each other.
Author contribution
All the authors met the standard writing criteria based on the
recommendations of the International Committee of Medical Journal Editors and
all contributed equally to the writing of the work.
Acknowledgments
We gratefully thank Dr. Shahram Taib, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran, for
their support and guidance.
Conflict of interest
The authors declare no competing interests.
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