The challenging issue of low dose radiation hormesis and adaptive response- findings from earth to space (Nov 17 2014)

Debate:
Non-Linear Dose Response
SMJ Mortazavi
Prof. of Medical Physics
Shiraz University of Medical Sciences
mmortazavi@sums.ac.ir
1

Paracelsus (1493-1541)
• "All substances are
poisons; there is none
which is not a poison.
• The right dose
differentiates a
poison…."
Mortazavi SMJ, Ph.D
2

Hormesis
• All chemical substances will exhibit a toxic
effect given a large enough dose.
• If the dose is low enough even a highly toxic
substance will cease to cause a harmful
effect.effect.
• The toxic potency of a chemical is thus
ultimately defined by the dose (the amount)
of the chemical that will produce a specific
response in a specific biological system.
• Source:
http://learn.caim.yale.edu/chemsafe/references/dose.html
Mortazavi SMJ, Ph.D
3

LNT & Radiation Hormesis
• The radiation hormesis model, unlike the LNT
model, assumes that adaptive/protective
mechanisms can be stimulated by low-dose
radiation and that they can prevent bothradiation and that they can prevent both
spontaneous and toxicant-related cancers as
well as other adverse health effects (Calabrese
et al. 2007).
Mortazavi SMJ, Ph.D
4

Natural radiation deficiency
symptoms
 It has been long
known that protozoa
and bacteria exposed
to artificially lowered
levels of naturallevels of natural
radiation
demonstrate
deficiency symptoms
expressed as
dramatically
decreased
proliferation.
Mortazavi SMJ, Ph.D
5

Mortazavi SMJ,
Ph.D
Radon & Lung Cancer in Ramsar, Iran
 Radon levels in some dwellings are up to 3700 Bq/m3
(over 100 pCi/L).

 The people and their ancestors exposed to abnormally
high radiation levels over many generations.
10
 If a radiation dose of a few hundred mSv per year is
detrimental to health causing genetic abnormalities or
an increased risk of cancer, it should be evident in these
people.
Mortazavi SMJ, M. Ghiassi-Nejad and M. Rezaiean. Cancer risk due to exposure to
high levels of natural radon in the inhabitants of Ramsar, Iran in: High Levels of
Natural Radiation and Radon Areas: Radiation Dose and Health Effects, T. Sugahara,
M. Morishima, M. Sohrabi, Y Sasaki, I. Hayata, and S. Akiba Eds, pp. 436-437,
Elsevier, Amsterdam, 2005.

Mortazavi SMJ,
Ph.D
Study Design
• Ramsar was divided into eight health districts
and a health center provided primary health
services in each health district.
• Indoor radon concentration levels were
11
• Indoor radon concentration levels were
previously measured in each dwelling by the
Iranian Nuclear Regulatory Authority experts.
Mortazavi SMJ, M. Ghiassi-Nejad and M. Rezaiean. Cancer risk due to exposure to
high levels of natural radon in the inhabitants of Ramsar, Iran in: High Levels of
Natural Radiation and Radon Areas: Radiation Dose and Health Effects, T. Sugahara,
M. Morishima, M. Sohrabi, Y Sasaki, I. Hayata, and S. Akiba Eds, pp. 436-437,
Elsevier, Amsterdam, 2005.

Mortazavi SMJ,
Ph.D
Cancer Mortality
• The overall cancer mortality, lung cancer
mortality and neonatal death rate of different
districts in the years from 2000 to 2001 were
collected.
12
collected.
• The radon prone houses were located in a district
named Ramak.
Mortazavi SMJ, M. Ghiassi-Nejad and M. Rezaiean. Cancer risk due to exposure
to high levels of natural radon in the inhabitants of Ramsar, Iran in: High Levels
of Natural Radiation and Radon Areas: Radiation Dose and Health Effects, T.
Sugahara, M. Morishima, M. Sohrabi, Y Sasaki, I. Hayata, and S. Akiba Eds, pp.
436-437, Elsevier, Amsterdam, 2005.

Mortazavi SMJ,
Ph.D
Surprising Results
• Our study showed that the highest lung cancer
mortality rate was in Galesh Mahaleeh, where the
radon levels were normal.
• On the other hand, the lowest lung cancer
mortality rate was in Ramak, where the highest
13
mortality rate was in Ramak, where the highest
concentrations of radon in the dwellings were
found
Mortazavi SMJ, M. Ghiassi-Nejad and M. Rezaiean. Cancer risk due to exposure to high
levels of natural radon in the inhabitants of Ramsar, Iran in: High Levels of Natural
Radiation and Radon Areas: Radiation Dose and Health Effects, T. Sugahara, M.
Morishima, M. Sohrabi, Y Sasaki, I. Hayata, and S. Akiba Eds, pp. 436-437, Elsevier,
Amsterdam, 2005.

Mortazavi SMJ,
Ph.D
Crude Lung
Cancer Rate
14
Amsterdam, 2005.

Mortazavi SMJ,
Ph.D
Adjusted
Lung Cancer
Rate
15
Amsterdam, 2005.

Mortazavi SMJ, Ph.D
16
The Study of Tumor Markers
in High Background Radiation Areas
Source:
S Taeb, SMJ Mortazavi, A Ghaderi, H Mozdarani, MR Kardan, SAR Mortazavi, A
Soleimani, I Nikokar, M Haghani, A Soofi. Alterations of PSA, CA15.3, CA125, Cyfra21-
1, CEA, CA19.9, AFP and Tag72 tumor markers in human blood serum due to long term
exposure to high levels of natural background radiation in Ramsar, Iran. International
Journal of Radiation Research. in press.

Why Tumor Markers?
• Recently, as no excess
cancer rate was reported
in these areas by
epidemiological studies,
we studied the tumor
Mortazavi SMJ, Ph.D
17
we studied the tumor
markers in the
inhabitants of these
areas to shed some light
on the impact of high
levels of background
radiation on cancer
induction.

Methods
• The level of background gamma radiation as well
as indoor radon was determined using RDS-110
and CR dosimeters.
• Thirty five individuals from a high background
radiation area (HBRA) and 35 individuals from a
Mortazavi SMJ, Ph.D
18
radiation area (HBRA) and 35 individuals from a
normal background radiation area (NBRA) were
randomly selected to participate in the study.
• Commercial ELISA kits (sandwich type ELISA
tests) were used to measure the serum levels of
PSA, CA15.3, CA125, Cyfra21-1, CEA, CA19.9,
AFP and Tag72 tumor markers.

Results
• Among the eight biomarkers investigated, the
means of PSA, CA15.3, CA125, CA19.9 and AFP
concentrations between the HBRAs and NBRAs
were not different.
• However, Cyfra21, CEA and Tag72 in HBRA group
Mortazavi SMJ, Ph.D
19
revealed significant increases compared to those of
NBRA group (P<0.05).
• Statistically significant correlation between the
external gamma dose as well as indoor radon level
and the concentration of CEA (P<0.001), Cyfra-
21(P<0.001) and TAG 72 (P<0.001 and 0.01
respectively) biomarkers were also observed.

What is Adaptive
Response?
RadiationIs it different from Radiation
Hormesis?
Mortazavi SMJ, Ph.D
20

Adaptive Response
When large radiation
exposure is preceded by
Mortazavi SMJ, Ph.D
21
exposure is preceded by
a small “tickle” dose, the
effect of the large dose is
sometimes diminished

Adaptive Response
70
80
90
When a small dose of radiation is given before a larger one, it would be
expected there would be more chromosome aberrations than when just
the large dose was given. But that is not what happens. With a small
“tickle” dose before the larger dose, there were only about half as many
aberrations than with just a large dose!
Intervention
09/01
0
10
20
30
40
50
60
0 0.5 150 0.5 + 150
Observed
Expected
Shadley and Wolff 1987
Dose cGy
Intervention

Adaptive Response Mechanisms
Small doses of radiation appear to:
 Stimulate protective responses
 Triggering DNA repair mechanisms
Mortazavi SMJ,
Ph.D
24
 Triggering DNA repair mechanisms
 Elimination of severely damaged
cells

Adaptive response is specific
There seems to be a genetic basis for
adaptive response, since it is
26
adaptive response, since it is
demonstrated only in specific cell
lines, tissues, animal lines and individuals.
It is demonstrated only for specific
biological changes.
Mortazavi SMJ, Ph.D

Genetic Basis? Mortazavi SMJ, Ph.D
27
Mortazavi SMJ, Ikushima T, and Mozdarani H. Variability of chromosomal radioadaptive
response in human lymphocytes. Iran. J. Radat. Res., 1(1): 55 - 61, 2003.

Genetic Basis? Mortazavi SMJ, Ph.D
28

Natural Radiation &
Adaptive Response
Mortazavi SMJ, Ph.D
29
High levels of natural
radiation can induce
adaptive responses

Mortazavi SMJ, Ph.D
30
Two survey meters show dose rates of 142 and 143
µSv/h on contact with a bedroom wall

Mortazavi SMJ, Ph.D
The 1st report on the
induction of adaptive
response in the residents of
High Background
Radiation Areas (HBRAs)
31
115 citations recorded by Web of
Science

Radiofrequency-Induced
Adaptive Response
Mortazavi SMJ, Ph.D
35

Radiofrequency-Induced Adaptive
Response
Mortazavi SMJ, Ph.D
36
• In 2009, it was found that pre-exposure of
cultured cells to radiofrequency radiation
induced an adaptive response which increased
the resistance of these cells to mytomycin C
(Sannino et al. , 2009a).

Radiofrequency-Induced Adaptive Response
 Mortazavi et al. also found that laboratory animals
pre-irradiated with radiofrequency radiation were
less susceptible to subsequent lethal effects of high
doses of ionizing radiation (Mortazavi et al. , 2011a,
Mortazavi et al. , 2012a).
Mortazavi SMJ, Ph.D
37
 These findings later confirmed by our subsequent
reports (Mortazavi et al. , 2011b, Mortazavi et al,
2012a) as well as the very limited published reports
that investigated the induction of adaptive response
after pre-treatment with microwave radiation (Cao
et al. , 2011, Jiang et al. , 2012, Sannino et al. ,
2009b, Sannino et al. , 2011, Zeni et al. , 2012).

 As indicated before, Sannino et al. had previously
reported that pre-exposure of peripheral blood
lymphocytes collected from human volunteers to non-
ionizing RF radiation (900 MHz, at a peak specific
absorption rate of 10 W/kg for 20 h) increases their
resistance to a challenge dose of mitomycin C (100
Mortazavi SMJ, Ph.D
40
resistance to a challenge dose of mitomycin C (100
ng/ml at 48 h) (Sannino, Sarti, 2009b).
 Later, they confirmed their previous results and
showed that the timing of adapting dose exposure of
radiofrequency plays an important role in the process
of adaptive response induction (Sannino, Zeni, 2011).
2012).

 On the other hand, Chinese researchers have
recently shown that pre-exposure of mice to non-
ionizing 900 MHz RF induced adaptive response and
thus reduced the hematopoietic tissue damage from
a subsequent challenge dose of ionizing radiation
Mortazavi SMJ, Ph.D
41
a subsequent challenge dose of ionizing radiation
(Cao, Xu, 2011).
 Zeni et al. also showed that when lymphocytes were
pre-exposed to RF at 0.3W/kg SAR and then treated
with mitomycin C, these cells showed a significant
reduction in the frequency of micronuclei, compared
with the cells treated with MMC alone (Zeni,
Sannino, 2012).

 Jiang et al. also recently used a relatively similar
method as we did previously (using the gamma
radiation as the challenge dose) and indicated that
mice pre-exposed to RF for 3, 5, 7 and 14 days showed
progressively decreased damage and were
significantly different from those exposed to gamma-
Mortazavi SMJ, Ph.D
42
significantly different from those exposed to gamma-
radiation alone (Jiang, Nie, 2012).
 It has also been reported that pre-exposure of Human
promyelocytic leukemia HL-60 cells to 900 MHz
radiofrequency radiation for 1 hour/day for 3 days
had a protective effect in hematopoietic tissue damage
induced by doxorubicin, a chemotherapeutic drug
(Jin et al. , 2012).

• More recently, Jiang et al. used the micronuclei
(MN) assay as the endpoint and showed that
exposure of mice to both adapting (900MHz RF
radiation) and challenge (3Gy gamma-
radiation) doses (AD+CD) resulted in a
Mortazavi SMJ, Ph.D
43
radiation) doses (AD+CD) resulted in a
significant decrease in MN indices compared to
those exposed to CD alone (Jiang et al. , 2013).

Mortazavi SMJ, Ph.D
44

Window Theory
Mortazavi SMJ, Ph.D
45

Mortazavi SMJ, Ph.D
RE Mitchel:
“the adaptive response in
mammalian cells and mammals
operates within a certain
window that can be defined by
46
window that can be defined by
upper and lower dose thresholds,
typically between about 1 and
100 mGy for a single low dose
rate exposure”
(Mitchel 2010)

Doxorubicin
• Doxorubicin (DOX or adriamycin) is the most
commonly used anticancer drug because of its
efficacy against various tumors.
Mortazavi SMJ, Ph.D
49
efficacy against various tumors.
• Like many other chemotherapeutic drugs,
administration of DOX has toxic effects on
hematopoietic cells
Jin et al. 2012

Minimum power density
• A preliminary experiment was conducted to
determine the minimum power density needed
for 900 MHz RF pre-exposure to minimize the
damage induced by subsequent exposure to
Mortazavi SMJ, Ph.D
50
damage induced by subsequent exposure to
DOX.
• Cells were pre-exposed to 900 MHz RF at 12,
120 and 1200 mW/cm2 power density for 1
hour/day for 3 days.
Jin et al. 2012

Mortazavi SMJ, Ph.D
51
Jin et al. 2012

Window Theory in Non-Ionizing Radiation-Induced
Adaptive Responses
Dear Editor,
I read with great interest an article by Jin et al. “The Effect of
Combined Exposure of 900 MHz Radiofrequency Fields and
Doxorubicin in HL-60 Cells", published in the Sep 2012 issue of
PLOS ONE Journal (Jin et al. 2012). The authors of the article
reported some interesting findings on the induction of adaptive
Mortazavi SMJ, Ph.D
53
reported some interesting findings on the induction of adaptive
response by pre-exposure of HL-60 Cells to radiofrequency (RF)
radiations. As summarized in Table 1, the viability of the cells
exposed to DOX alone was 70.2 ± 0.2 while when cells were exposed
to 900 MHz RF radiation at 12 ìW/cm2 before treatment with DOX,
the viability was 82.8 ± 2.1 (P<0.01). RF exposure at higher power
densities significantly decreased the viability (60.7 ± 0.5 and 58.6 ±
0.5 for 120 ìW/cm2 and 1200 ìW/cm2, respectively). On the other
hand they reported that they had previously conducted a preliminary
experiment to determine the minimum power density for RF pre-
exposures to minimize the damage induced by subsequent exposure
to DOX.

Non-responsiveness Phenomenon
Lack of AR in Some Individuals
Mortazavi SMJ, Ph.D 54
Reported by:
•Ikushima, T., and Mortazavi SMJ. Radioadaptive response: its
variability in cultured human lymphocytes, In: Biological effects
of low dose radiation, Yamada T, Mothersil C, Mich BD and
Potten CS (eds), pp 81-86, 2000.
•Mortazavi SMJ, Ikushima T, and Mozdarani H. Variability of
chromosomal radioadaptive response in human lymphocytes. Iran.
J. Radat. Res., 1(1): 55 - 61, 2003.

Immunological Implications
of
RF-Induced Adaptive
Response
Mortazavi SMJ, Ph.D
55
Response

Immune System & Space Research
 Immune system is highly susceptible to different stressors
exist during space flight (Gridley et al. , 2009).
 Dysregulation of the immune system during and
immediately following space missions (Crucian et al. ,
2011, Crucian et al. , 2008).
Mortazavi SMJ, Ph.D
56
 Despite the well-known reversible immunological
alterations in short-term spaceflights, the bioeffects of
long-duration spaceflight on neuroimmune responses
have not been completely known so far (Stowe et al. ,
2011).
 Solar and galactic radiation are associated with increased
risk of infection during long term stay of human outside
the Earth’s magnetic field (Zhou et al. , 2012).

Implications of
RF-Induced Adaptive Response
• Mortazavi et al. have also recently shown that
pre-exposure of BALB/c mice to radiofrequency
radiation emitted from a GSM mobile phone
Mortazavi SMJ, Ph.D
57
radiation emitted from a GSM mobile phone
increases their resistance to a subsequent
bacterial infection (E. coli infection) (Mortazavi
et al. , 2012b).

Implications of
RF-Induced Adaptive Response
 Although there is a report by Plews et al. that indicates
the induction of adaptive response induced by low-dose
whole-body radiation treatments prolonged the
survival of prion-infected mice by reducing oxidative
Mortazavi SMJ, Ph.D
58
survival of prion-infected mice by reducing oxidative
stress (Plews et al. , 2010), to the best of our knowledge
our study was the first study which showed the
induction of adaptive response as prolonged survival of
Escherichia coli-infected BALB/c mice by pre-exposure
to radiofrequency radiation (non-ionizing radiation).

Mortazavi SMJ, Ph.D
62
Source:
Mortazavi SMJ, Motamedifar M, Mehdizadeh AR, Namdari G, Taheri M. The Effect of Pre-exposure to
Radiofrequency Radiations Emitted from a GSM Mobile Phone on the Suseptibility of BALB/c Mice to
Escherichia coli. Journal of Biomedical Physics and Engineering. 2012; 2(4):139-46.

Adaptive Response in Space Research
• Concluding Remark:
• Exposure of astronauts to continuous isotropic
galactic cosmic radiation or low levels of
radiofrequency radiation can increase their
Mortazavi SMJ, Ph.D
63
resistance against solar particle events or
infections caused by life-threatening
microorganisms.

Implications of RF-Induced
Adaptive Response in
Space Research
Mortazavi SMJ, Ph.D
64

Adaptive Response in Space
Research
 In a report entitled “Adaptive response studies may
help choose astronauts for long-term space travel”,
which published in "Advances in Space Research"
(Mortazavi et al. , 2003), it was previously
Mortazavi SMJ, Ph.D
65
(Mortazavi et al. , 2003), it was previously
hypothesized that screening of the candidates of deep
space missions by Ground-based in vitro adaptive
response tests before any mission can be used to
identify the individuals who respond well to low levels
of ionizing radiation and reveal high magnitudes of
radioadaptive response (Mortazavi et al. , 2005).

Mortazavi SMJ, Ph.D
66
2003
23 citations
according to Scopus

Two years after Mortazavi et al 2003
report, NASA agrees that adaptive
response is a puzzling issue in space
radiobiology
• 2005-Cancer specialist Dr. John
Dicello
• “Cells often react in unexpected ways to radiation, notes Dicello.
Mortazavi SMJ, Ph.D
68
• “Cells often react in unexpected ways to radiation, notes Dicello.
For example, there's a puzzling phenomenon known as adaptive
response. Sometimes, when tissue is exposed to damaging
radiation, it not only repairs itself, but also learns to repair itself
better next time. How that works is still being investigated”
• “The damage could be less than the two kinds added together -- or
it could be more! There could, perhaps, be an adaptive response in
which lightweight solar protons stimulate repair processes to help
reduce the effects of the heavy cosmic ray ions. Or something
totally unexpected could happen”.
• Mysterious Cancer http://science.nasa.gov/

Mortazavi SMJ, Ph.D
69
Four years
after
Mortazavi
et al 2003
George et al. 2007:
“This study of adaptive response is very interesting and it is important
that the phenomenon be investigated further.
et al 2003
report, in
2007:

Mortazavi SMJ, Ph.D
70
• Durante and Manti 2008:
• “Another possibility is that an adaptive response to the space environment takes
place after the first exposure, which may confer the exposed individual an increased
radioresistance. Such a response would be similar to that hypothesized to explain
the apparent lack of adverse health effects in VHBRA and HBRA residents. As
pointed out by Mortazavi et al. (2003), radiobiological studies on these areas may
lead to the identification of the cellular and molecular mechanisms by which
susceptibility to genetic damage and cancer is decreased by chronic radiation
exposure, hence helping the astronaut selection process.”

Mortazavi SMJ, Ph.D
72
Mortazavi et al., Advances in Space Research, Vol 31, No. 6, 1543-1552, 2003

RF-Induced
Adaptive
Response in
Space
Research
• Different
Mortazavi SMJ, Ph.D
73
• Different
methods that
can be used for
reducing the
risk of
radiation
during deep
space missions

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Mortazavi SMJ, Ph.D
77
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Mortazavi SMJ, Ph.D
79
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