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Very high background radiation areas of Ramsar, Iran: Preliminary biological
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Paper
VERY HIGH BACKGROUND RADIATION AREAS OF RAMSAR,
IRAN: PRELIMINARY BIOLOGICAL STUDIES
M. Ghiassi-nejad,*†
S. M. J. Mortazavi,*‡
J. R. Cameron,§
A. Niroomand-rad,࿣
and
P. A. Karam¶
Abstract—People in some areas of Ramsar, a city in northern
Iran, receive an annual radiation absorbed dose from background
radiation that is up to 260 mSv y؊1
, substantially
higher than the 20 mSv y؊1
that is permitted for radiation
workers. Inhabitants of Ramsar have lived for many generations
in these high background areas. Cytogenetic studies show
no significant differences between people in the high background
compared to people in normal background areas. An
in vitro challenge dose of 1.5 Gy of gamma rays was administered
to the lymphocytes, which showed significantly reduced
frequency for chromosome aberrations of people living in high
background compared to those in normal background areas in
and near Ramsar. Specifically, inhabitants of high background
radiation areas had about 56% the average number of induced
chromosomal abnormalities of normal background radiation
area inhabitants following this exposure. This suggests that
adaptive response might be induced by chronic exposure to
natural background radiation as opposed to acute exposure to
higher (tens of mGy) levels of radiation in the laboratory.
There were no differences in laboratory tests of the immune
systems, and no noted differences in hematological alterations
between these two groups of people.
Health Phys. 82(1):87–93; 2002
Key words: health effects; naturally occurring radionuclides;
radiation, background; exposure, population
INTRODUCTION
LIFE EVOLVED in an environment with higher radiation
levels than exist today, and background radiation levels
today are lower than at any time in the history of life on
Earth. Since life first evolved, background radiation
levels have decreased by a factor of about 10, although
there has been a negligible reduction since the evolution
of humans (Karam and Leslie 1999). At present, natural
background radiation levels on Earth vary by at least two
orders of magnitude today, so humans and other organisms
are subject to a wide range of background radiation
levels. The annual background doses in some areas of the
world are given in Table 1. These do not include
contributions from radon progeny in the lungs, which are
estimated to be even greater than the absorbed doses
shown if the radiation weighting factor of alpha particles
is taken into account. Areas with unusually high background
(high background radiation areas, or HBRAs) are
found in Yangjiang, China; Kerala, India; Guarapari,
Brazil; and Ramsar, Iran. Some areas of Ramsar, a city in
northern Iran, have among the highest known background
radiation levels in the world. For the purposes of
this paper, “dose” will be used to mean absorbed beta/
gamma radiation dose because the contribution of alpha
emitters is not considered.
The high background radiation in the “hot” areas of
Ramsar is primarily due to the presence of very high
amounts of 226
Ra and its decay products, which are
brought to the Earth’s surface by hot springs. Groundwater
is heated by subsurface geologic activity and
passes through relatively young and uraniferous igneous
rock. Radium is dissolved from the rocks by hot ground
water. Uranium is not dissolved because the groundwater
is anoxic and uranium is insoluble in anoxic waters
(Langmuir 1978; Grandstaff 1976). When the groundwater
reaches the surface at hot spring locations, travertine,
a calcium carbonate mineral, precipitates out of solution
with dissolved radium substituting for calcium in the
mineral. A secondary cause of high local radiation levels
is travertine deposits with a high thorium concentration
(Sohrabi 1990). The radioactivity in local soils and the
food grown in them are also high because soils are
derived from the weathering of local bedrock. Table 2
details the range of radioactivity levels measured in some
local rocks and soil samples.
There are at least nine known hot springs with
various concentrations of radioactivity around Ramsar.
Residents and visitors use these springs as health spas.
Residents of these “hot” areas have also used the residue
of the hot springs as building materials to construct
* National Radiation Protection Department, Iranian Nuclear
Regulatory Authority, P.O. Box 14155-4494, Tehran, Iran; †
Biophysics
Department, Tarbiat Modares University, Tehran, Iran; ‡
Medical
Physics Department, School of Medicine, Rafsanjan University of
Medical Sciences, Rafsanjan, Iran; §
Departments of Medical Physics,
Radiology, and Physics, University of Wisconsin, Madison, WI;
࿣
Department of Radiation Medicine, Georgetown University, LL Bles
Building, 3800 Reservoir Road, Washington, DC 20007-2197;
¶
Department of Environmental Medicine, University of Rochester,
601 Elmwood Ave Box HPH, Rochester, NY 14642.
For correspondence or reprints contact: S. M. J. Mortazavi,
Biology Division, Kyoto University of Education, Kyoto 612-8522,
Japan, or email at mortazar@kyokyo-u.ac.jp.
(Manuscript received 5 January 2001; revised manuscript received
23 April 2001, accepted 5 August 2001)
0017-9078/02/0
Copyright © 2002 Health Physics Society
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87
houses. The indoor and outdoor gamma radiation absorbed
dose rates in some parts of Ramsar range from 50
to 900 ␮Gy hϪ1
, although other areas in the city have
absorbed dose rates that are much lower. The annual dose
to monitored individuals ranges up to 132 mGy, and we
have calculated maximum credible annual radiation exposures
of up to 260 mGy. The recommended dose limit
for workers in Iran is 20 mSv yϪ1
, so some residents in
the Ramsar area receive a much higher annual radiation
exposure than is permitted for radiation workers. Figs. 1
and 2 show the location of Ramsar and the highest
background radiation areas with respect to populated
areas.
The people who live in high radiation areas of the
world are of considerable interest because they and their
ancestors have been exposed to abnormally high radiation
levels over many generations. If an annual radiation
exposure of a few hundred mSv is detrimental to health,
causes genetic abnormalities, or an increased risk of
cancer, it should be evident in these people, given a large
enough population to study. A description of our study
methods and results follows.
METHODS
Following is a brief description of the methods
employed for testing accomplished to date.
Potential participants were identified from residents in
areas of normal (14 persons) and elevated (21 persons)
background radiation levels of Ramsar. After description of
Table 1. Mean and maximum annual background absorbed doses (mGy yϪ1
) to the inhabitants of some areas of the
world from geologic and cosmic radiation. The areas in Iran, India, Brazil, and China are all due to local geologic and
geochemical effects, giving rise to very high and very localized radiation exposure. The other elevated radiation areas
noted stem largely from the presence of large-scale geologic formations such as granitic mountain ranges, widespread
geothermal activity, and so forth. (1) Radiation Research Foundation, Kyoto, Japan (used with permission of Radiation
Research Foundation); (2) UNSCEAR (2000); (3) UNSCEAR (2000) reports maximum dose rates of 789 mGy yϪ1
on
beaches of monazite sands. The levels reported here are those found in the city itself; (4) Only mean exposure
information is provided in the reference noted.
Area, Country
Mean dose
(mGy yϪ1
)
Maximum dose
(mGy yϪ1
)
Minimum dose
(mGy yϪ1
)
Ramsar, Iran 260 (1) 0.61
149 (2)
Kerala, India 35 1.75
Guarapari, Brazil (3) 1.49 0.79
Yangjiang, China (2, 4) 3.24
Ireland (2) 0.37 1.58 0.01
Austria (2) 0.38 1.31 0.18
USA (2) 0.41 1.03 0.12
Germany (2) 0.44 3.07 0.04
Denmark (2) 0.46 0.61 0.31
Japan (2) 0.46 0.67 0.18
India (2) 0.49 9.64 0.18
China (2) 0.50 0.76 0.15
France (2) 0.60 2.19 0.09
Iran (2) 0.62 1.14 0.32
Norway (2) 0.64 10.52 0.18
Italy (2) 0.65 2.00 0.03
Hong Kong (2) 0.76 1.05 0.45
World Average (2) 0.50 0.82 0.16
Table 2. Analytical results from Ramsar plants and geologic media. All results are in Bq gϪ1
with the 95% confidence
intervals in parentheses. All analytical results are from Esmaili and Asgharnejad (2002). It is particularly interesting to
note the difference in thorium and radium radioactivity concentrations. This is due to the different solubility of these two
elements in water; radium (particularly in the form of RaCl) is very soluble while thorium is relatively insoluble.
Location No. of samples 226
Ra 232
Th 40
K
Lamtarmaballeh 5 53.9 (8.2) 17.2 (2.0) 385.5 (18.5)
Ramak 3 5700.0 (93.4) 120.0 (20.0) 418.0 (62.0)
Gharmirh 5 110.5 (88.1) 32.2 (8.9) 423.0 (132.0)
Sadalmahelleh 4 127.0 (2.0) 28.3 (1.6) 296.0 (41.0)
Sefid Tamcahk 6 20.9 (3.2) 21.2 (2.2) 265.0 (81.0)
Lapasar 5 25.6 (2.0) 26.7 (11.7) 425.7 (92.0)
Chaparsar 11 114.1 (7.3) 15.7 (3.2) 634.0 (38.6)
Khake’safied 6 38,000 (10,000) 25.2 (1.8) 235.0 (82.2)
Talesh Mahalleh 15 19,000 (11,000) 43.5 (16.8) 436.6 (134.5)
Local stone (normal) 461.0 (11.5) 20.1 (2.8) 365.0 (51.0)
Travertine stone 421,000 (3000) 22.8 (4.1) 138.1 (22.0)
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88 Health Physics January 2002, Volume 82, Number 1
the study and its objectives to the participants, they were
asked to complete questionnaires, participate in interviews,
allow radiation measurements of their homes, and to submit
blood samples. Every attempt was made to match data from
the HBRA participants with corresponding ones from the
normal background radiation area (NBRA) participants in
as many aspects as possible, although this was not always
feasible. Most families in this part of Iran have lived in the
same geographic area for many generations, often remaining
in the same house their entire lives. We are in the
process of collecting detailed information from study participants
on their family histories regarding moving to and
within Ramsar; this information will be included with our
final results.
Cell and chromosome studies
Venous blood samples were drawn from healthy
donors of both sexes who lived in high background areas
(HBRAs) or a neighboring normal background radiation
area (NBRA) into heparinized vacutainers. The blood
was cultured in culture flasks at 37°C. Fifty-two hours
after phytohemagglutinin (PHA) stimulation, colcemid
was added to arrest the dividing lymphocytes in mitosis.
At 54 h, the cells were harvested. Metaphases with 46
Fig. 1. A map of Iran showing the location of Ramsar. The city lies between the Elburz Mountains and the Caspian Sea
at an average elevation near sea level (the Caspian Sea is about 30 m lower than sea level). As noted in the text, this
region is geologically young with an abundance of subsurface geothermal activity that is directly responsible for the
elevated radiation levels present.
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89Very high background radiation areas of Ramsar, Iran ● M. GHIASSI-NEJAD ET AL.
chromosomes were scored and the frequency of chromosome
aberrations determined.
Hematological studies
Healthy blood donors from HBRAs of Ramsar as
well as a neighboring NBRA were selected. Blood cell
counts were performed by a Data Cell 20 machine.
Immunological studies
Healthy blood donors from HBRAs and a neighboring
NBRA were selected. Serum concentrations of different
immunoglobulin classes were determined by Single
Radial Immuno Diffusion (SRID) method.
Adaptive response studies
At least 200 lymphocytes from each blood sample
were analyzed for chromosomal aberrations according to
the procedure noted above, after which the blood samples
were then exposed only to a challenge dose of 1.5 Gy
(i.e., no conditioning dose was given). The cells were
exposed to the challenge dose of 1.5 Gy of gamma rays
48 h after PHA stimulation. The background level of
chromosomal aberrations (i.e., before the conditioning
dose was administered) in all residents was similar.
Following exposure to the challenge dose, 200 lymphocytes
from each participant were analyzed for the number
of chromosomal aberrations and these results were averaged
to determine the mean number of chromosomal
aberrations per cell (reported as MCAPC).
RESULTS
Cancer incidence and life expectancy
Although there is not yet solid epidemiological
information, most local physicians in Ramsar report
anecdotally there is no increase in the incidence rates of
Fig. 2. A map of the HBRA in Ramsar. The areas of highest background are found in discrete locations, corresponding
to specific geologic features. Other areas of elevated background radiation levels are found elsewhere in the city; these
are the highest levels found in residential areas. Although the locations of individual houses are not noted on this map,
the entire area is residential, and 1–2 family houses are spaced about 20–30 m apart along each of the roads shown. On
this map, one inch is equal to a distance of about 100 m.
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90 Health Physics January 2002, Volume 82, Number 1
cancer or leukemia in their area (Mortazavi 2002). The
life span of HBRA residents also appears no different
than that in residents of nearby NBRAs, although this
information is, again, anecdotal at this time. Such findings,
if confirmed, are in keeping with the results of
previous studies of HBRA residents and radiation workers
(for example, Ikushima 1999; Chen and Wei 1991;
Smith and Doll 1981).
Adaptation to radiation stress
It is known that cellular damage from a small
amount of ionizing radiation and a variety of DNA
damaging agents, such as UV, alkylating or oxidizing
agents, and heat, can induce repair responses (Ikushima
et al. 1996; Ikushima and Mortazavi 2002). The results of
many studies indicate that when cells are exposed to low
doses of stressing agents, they often become less sensitive
to the harmful effects of a subsequent higher dose
(Ikushima et al. 1996). This type of induced repair is
called an adaptive response.
Our studies showed 56% fewer MCAPC resulting
from the challenge dose among high background residents
compared to lymphocytes from residents of neighboring
low background areas (p Ͻ 0.001). These results
are in keeping with those reported by Mitchell and
Boreham (2000) in laboratory studies. We feel these
results are intriguing because no overt conditioning dose
was given to Ramsar residents; in this case, the “conditioning”
dose was exposure to the natural background
radiation in the Ramsar HBRA. The results of these
studies are shown in Figs. 3, 4, and 5.
Hematological studies
Beginning in 1999, the National Radiation Protection
Department of the Iranian Nuclear Regulatory Authority
performed an integrated multi-disciplinary study
on the health effects of relatively high levels of natural
radiation in some areas of Ramsar. The main purpose
was to look for hematological changes due to prolonged
high background radiation. Healthy volunteers of both
sexes from high background and neighboring normal
background areas in Ramsar were examined for changes
in the following hematological parameters: counts of
white blood cells (leukocytes), lymphocytes, monocytes,
granulocytes, and erythrocytes (red blood cells); measurements
of hemoglobin, hematocrit, mean corpuscular
volume (MCV), mean corpuscular hemoglobin (MCH),
mean corpuscular hemoglobin concentration (MCHC),
red cell distribution width (RDW), platelet, and mean
platlet volume (MPV). As noted above, our results
indicate there are no statistically significant differences
between the two groups of participants in all these
hematological parameters.
Fig. 3. Mean chromosome aberrations per cell (MCAPC) among
21 inhabitants of high background radiation areas (HBRA) and 14
living in normal background radiation areas (NBRA). Note that the
95% confidence intervals for these two populations overlap,
indicating there is no statistically significant difference in the level
of background chromosomal abnormalities in these two popula-
tions.
Fig. 4. MCAPC among individuals who live in the Ramsar HBRA
and the average of 14 from a nearby control area. Persons 1 and 2
are married and live in a house with radiation levels of about 20
␮Gy hϪ1
in the bedroom, giving an average annual radiation dose
of 58.4 mGy yϪ1
simply from sleeping. Person 3 has a hot spring
in her house with radiation levels of up to 50 ␮Gy hϪ1
. Each data
point is based on analysis of 200 cells per person obtained during
two separate sampling events. Note that, as in Fig. 1, the 95%
confidence intervals all overlap, suggesting that the number of
background chromosome abnormalities in these people are statistically
similar.
Fig. 5. MCAPC in irradiated and non-irradiated cells from inhabitants
of HBRAs and NBRAs. Samples from inhabitants of both
areas were examined for chromosomal abnormalities before and
after irradiation with 1.5 Gy. Although there is no statistically
significant difference in chromosomal abnormalities in both populations
before irradiation, there is a statistically significant difference
in post-irradiation abnormalities. In this case, cells from
inhabitants of the HBRAs have fewer chromosomal abnormalities
than those of inhabitants of NBRAs. Adaptive response has
previously been noted in organisms exposed to acute conditioning
doses at relatively high exposure rates; these results suggest that
chronic exposure to lower exposure rates may stimulate adaptive
response as well.
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91Very high background radiation areas of Ramsar, Iran ● M. GHIASSI-NEJAD ET AL.
Immunological studies
It is well known that high doses of ionizing radiation
can suppress the immune system (Anderson et al. 1980;
Celer 1990). On the other hand, some have suggested
low doses can stimulate the immune system (e.g.,
Feinendegen et al. 1998; Mine et al. 1990). Studies were
done to assess the effects of high background radiation
on immune parameters. Blood samples were obtained
from healthy individuals living in both high background
and neighboring normal background areas. The following
studies were done: concentration of serum immunoglobulins:
immunoglobulin A (IgA), immunoglobulin G
(IgG), immunoglobulin M (IgM), and complement components
3 and 4 (C3 and C4). Our findings showed a
slight increase in IgA and IgG levels of residents from
high, compared to normal, background areas. IgM, C3
and C4 complements were in the normal range for both
groups. Although increases in IgA and IgG were not
sufficient to show enhanced immune function, it is clear
that high doses of natural radiation are not immunosuppressive.
More research is needed to clarify the immunological
alterations induced by different levels of natural
radiation.
PRELIMINARY OBSERVATIONS
Although the long-term epidemiological studies of
Ramsar residents are currently in progress, we report
here some of the preliminary results of the cellular
studies. Figs. 3, 4, and 5 show these preliminary results,
which are based on the analysis of blood samples from 21
people living in the Ramsar HBRA and 14 controls from
a nearby NBRA. On the basis of our preliminary data, we
believe the following remarks are suitable:
1. These tests show no statistically significant difference
in chromosome abnormalities at the 95% confidence
level between these two groups (Fig. 3).
2. Blood samples from three individuals from an extraordinary
HBRA (external gamma dose was up to
155 ␮Gy h
Ϫ1
) and 14 persons from a nearby NBRA
also show no difference in the number of mean
chromosome aberrations per cell (MCAPC). These
results are based on examining 200 cells per person
obtained during two separate sampling events (Fig. 4).
3. Some blood samples from both HBRAs and NBRAs
were exposed to a challenge dose of 1.5 Gy. The
purpose of the challenge dose is to induce radiogenic
chromosomal abnormalities; cells demonstrating
adaptive response will have fewer chromosomal abnormalities
than those that do not have an adaptive
response. In this case, the confidence intervals do not
overlap and there is a statistically significant reduction
in chromosomal abnormalities following this
challenge dose among the residents of the HBRAs
(Fig. 5). Specifically, HBRA residents’ cells had an
average of 0.098 chromosomal aberrations per cell
following this exposure compared to 0.176 aberrations
noted in cells from residents of NBRAs.
4. Previous studies of adaptive response have concentrated
on stimulating effects with acute, relatively
high doses of radiation (UNSCEAR 1994). The results
shown in Fig. 5 suggest that chronic exposure to
relatively low levels of natural radiation may also
induce adaptive response. Further, it is possible that
continual radiation exposure may help to overcome
the relatively short adaptive response “half-life” that
has been reported.
DISCUSSION AND CONCLUSIONS
Cytogenetic analysis of chromosome aberrations in
peripheral blood lymphocytes is widely used to quantify
dose from radiation and other clastogens (Hoffmann and
Schmitz-Feuerhake 1999). Our preliminary cytogenetic
studies indicate no statistically significant difference in
chromosomal abnormalities between residents of the
HBRAs and people in control areas. It is worth noting
that our preliminary results do not agree with that
reported by Fazeli (1990) for residents in high background
areas. This needs further investigation. However,
on the basis of these preliminary results, we argue that
the risk from the high levels of natural background
radiation found in Ramsar may be less than the predictions
of linear no-threshold or supra-linear models of
radiation dose-response. We would also like to note that
the annual absorbed radiation dose to some residents of
Ramsar are significantly higher than the recommended
limit for the general public under ICRP recommendations
and Iranian regulations. In some cases, these levels
are even higher than the ICRP-recommended annual
limits for radiation workers (ICRP 1990).
In addition, we note that the chromosomal aberration
studies reported here, if borne out by research
currently underway, suggest that radioadaptive response
may be initiated by long-term exposure to relatively low
levels of ionizing radiation. Previous experiments in
adaptive response had looked primarily at the effects of
acute exposure to relatively high levels of radiation, and
the effects decreased over a period of days, as reported
by the United Nations Scientific Committee on the
Effects of Atomic Radiation (UNSCEAR 1994). The
stimulation of adaptive response by elevated levels of
natural background radiation suggests a plausible evolutionary
origin for this effect.
Please note that adaptive response (AR) refers to the
observation that exposing cells or some organisms to
relatively low “conditioning” doses of radiation prior to
exposure to a much higher “challenge” dose results in a
reduction in observed radiation effects (e.g., chromosomal
aberrations, death, etc.). By comparison, hormesis
is the induction of beneficial effects (e.g., reduction in
cancer rates, increase in life span) resulting from exposure
to a small amount of an agent. Our preliminary
studies seem to indicate the presence of adaptive response
in the cells of some Ramsar residents, but we do
not claim to have seen hormetic effects in any of those
studied.
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92 Health Physics January 2002, Volume 82, Number 1
Given the apparent lack of ill effects among observed
populations of these high dose rate areas, these
data suggest that current dose limits may be overly
conservative. However, the available data do not yet
seem sufficient to cause national or international advisory
bodies to change their current conservative radiation
protection recommendations; for this to happen more
definitive data are needed (Roth et al. 1996).
Radio-epidemiological studies of the residents of
high background areas, such as Ramsar, will provide
useful supporting data. The population in the high
background areas of Ramsar is estimated to be about
2,000 persons. To obtain statistically reliable results, a
long-term study will be needed to provide sufficient
person-years of observation. The life span of residents of
the high background areas of Ramsar should be a part of
future long-term studies. In time, we plan to extend our
study to include residents of Iran living in other areas
that, while not as high-dose as Ramsar, are still well
above the global average radiation dose. We feel that
these factors will make it possible to examine a wider
portion of the dose-response curve than is possible in any
other location on Earth.
Acknowledgments—The authors thank Professor Takaji Ikushima for
helpful discussions and critical reading of the manuscript.
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