Central nervous system lymphoma and radiofrequency radiation - A case report and incidence data in the Swedish Cancer Register on non-Hodgkin lymphoma

Abstract

Earlier animal studies have provided evidence that non-Hodgkin lymphoma (NHL) may be caused by exposure to radiofrequency (RF) radiation. This was recently confirmed by the U.S. National Toxicology (NTP) study that showed an increased incidence of malignant lymphoma in female mice exposed to the GSM modulated or the CDMA modulated cell phone RF radiation. Primary central nervous system lymphoma (PCNSL) is a rare malignancy in humans with poor prognosis. An increasing incidence has been reported in recent years. Based on a case-report we present the hypothesis that use of the hand-held mobile phone may be a risk factor for PCNSL. The increasing incidence of non-Hodgkin lymphoma in Sweden is discussed in relation to etiologic factors.

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Medical Hypotheses
journal homepage: www.elsevier.com/locate/mehy
Central nervous system lymphoma and radiofrequency radiation –A case
report and incidence data in the Swedish Cancer Register on non-Hodgkin
lymphoma
Lennart Hardell
a,b,⁎
, Michael Carlberg
b
, Tarmo Koppel
c
, Marie Nordström
d
, Lena K. Hedendahl
b
a
Department of Oncology, Faculty of Medicine and Health, Örebro University, SE-701 82 Örebro, Sweden
b
The Environment and Cancer Research Foundation, Studievägen 35, SE-702 17 Örebro, Sweden
c
Department of Labour Environment and Safety, Tallinn University of Technology, SOC353, Ehitajate tee 5, 19086 Tallinn, Estonia
d
Stockholm Sjukhem Foundation, Mariebergsgatan 22, 112 19 Stockholm, Sweden
ARTICLE INFO
Keywords:
Central nervous system lymphoma
Risk factors
Radiofrequency radiation
Incidence non-Hodgkin lymphoma
ABSTRACT
Earlier animal studies have provided evidence that non-Hodgkin lymphoma (NHL) may be caused by exposure to
radiofrequency (RF) radiation. This was recently confirmed by the U.S. National Toxicology (NTP) study that
showed an increased incidence of malignant lymphoma in female mice exposed to the GSM modulated or the
CDMA modulated cell phone RF radiation. Primary central nervous system lymphoma (PCNSL) is a rare ma-
lignancy in humans with poor prognosis. An increasing incidence has been reported in recent years. Based on a
case-report we present the hypothesis that use of the hand-held mobile phone may be a risk factor for PCNSL.
The increasing incidence of non-Hodgkin lymphoma in Sweden is discussed in relation to etiologic factors.
Introduction
Primary central nervous system lymphoma (PCNSL) is a rare ma-
lignancy with poor prognosis (survival usually < 1 year) [1]. The
annual incidence rate has been reported to vary between 7 cases per
1,000,000 persons in USA [2] and 0.2 cases per 100,000 person-years in
high income countries [3]. An increased lymphoma risk has been
identified among severely immunodeficient patients such as HIV-in-
fected or organ transplant individuals [4–6].
An increasing trend in PCNSL among HIV un-infected and non-
transplant persons was reported from USA. In men and women
aged + 65 years the incidence increased during 1992–2011 with 1.7%
and 1.6%/year, respectively, which was statistically significant [7].In
other age groups the incidence was stable. In a Swedish study on PCNSL
diagnosed 2000–2013 the average annual increase was 4%, 95% con-
fidence interval (CI) = 1.01–1.06. It was more pronounced in subjects
aged 70 + with average annual increase 6%, 95% CI = 1.02–1.10 [3].
Hypothesis
The etiology of the increasing incidence of PCNSL among persons
with no HIV or no organ transplantation is unknown. One factor that
has not been discussed so far is exposure to radiofrequency (RF) fields
to the brain during use of the handheld mobile phones and cordless
phones (DECT). We discuss it further based on a case report and we
hypothesize that the increasing incidence of PCNSL may be caused by
exposure to RF fields. We obtained informed consent by the patient to
review the medical records.
Methods
We analysed non-Hodgkin lymphoma (NHL) incidence per 100,000
person-years age-adjusted according to the World population for the
time period 1970–2017. The database what updated until 2018, but the
year 2018 was excluded due to missing cases according to the Swedish
Cancer Register (note in the online database). We selected ICD-7 codes
200 + 202 for NHL in the register administered by the National Board
of Health and Welfare (https://sdb.socialstyrelsen.se/if_can/val.aspx).
Statistical methods
The Joinpoint Regression Analysis program, version 4.7.0.0 was
used to examine incidence per 100,000 person-years in the Swedish
Cancer Register, by fitting a model of 0–5 joinpoints using permutation
tests with Bonferroni correction for multiple testing to calculate the
number of joinpoints that best fit the material [8]. When joinpoints
https://doi.org/10.1016/j.mehy.2020.110052
Received 23 April 2020; Accepted 25 June 2020
⁎
Corresponding author at: The Environment and Cancer Research Foundation, Studievägen 35, SE 702 17 Örebro, Sweden.
E-mail addresses: lennart.hardell@environmentandcancer.com (L. Hardell), tarmo@koppel.ee (T. Koppel).
Medical Hypotheses 144 (2020) 110052
0306-9877/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
T

were detected annual percentage changes (APC) and 95% confidence
intervals (CIs) were calculated for each linear segment. Average annual
percentage changes (AAPC) were also calculated for the whole time
period using the average of the APCs weighted by the length of the
segment.
Results
Case-report
A female case aged 53 years was in 2006 diagnosed with PCNSL of
diffuse large B-cell type. According to CAT scan it was a multilobular
tumour with central necrosis located in the right temporo-parieto-oc-
cipital region, see Fig. 1. There was a 10 mm deviation of the brain
midline to the left with compression of the ventricular system. The
patient was treated with primary surgery, chemotherapy, autologous
bone marrow transplantation and local radiotherapy. She survived
5 years and 3 months.
The patient had since early 1990’s used a GSM mobile phone (global
system for mobile communication) in her administrative work. She
used always her right hand and had no hands-free device. The mobile
phone was provided by her employer and her cumulative use during
working time was reported to be about 13,200 h (roughly 4 h per day).
Fig. 2 shows the RF field superimposed on the CAT scan, based on
calculations of depth of 900 MHz GSM mobile phone radiation [9, with
courtesy].
Incidence of NHL
In the Swedish Cancer Register the AAPC of the NHL incidence in
men increased during 1970–2017 with 1.66%, 95% confidence interval
(CI) + 1.40, +1.91%, with two joinpoints, in 1990 and 2005, Table 1
and Fig. 3. The corresponding result in women was +1.31%, 95%
CI + 0.92, +1.70%, with two joinpoints, 1977 and 1988, Table 2 and
Fig. 4. During the 1970′s and 1980′s a substantial statistically sig-
nificant increase in the incidence was seen in both genders. In both men
and women, the incidence increased statistically significant also during
2005–2017 and 1988–2017, respectively, but to a lower degree. Un-
fortunately, it is not possible to analyze the incidence of PCNSL using
the Swedish Cancer Register online database.
Consequences of the hypothesis and discussion
This patient had a typical PCNSL of diffuse large B-cell type. She had
no known risk factors such as HIV (tested HIV negative) or organ
transplant. She underwent multidisciplinary treatment resulting in
fairly long survival.
PCNLs in HIV-infected patients and organ transplant subjects are
associated with Epstein-Barr virus (EBV) whereas interaction with EBV
is uncommon in immunocompetent subjects [10]. Based on the ques-
tionnaire this patient did not report any pesticide exposure and she had
no organ transplant or intake of immunosuppressive drugs.
The patient reported a reasonable amount of RF radiation exposure
from a GSM hand-held mobile phone. She reported more than 13,000 h
of total use, with a latency time (tumour induction period) of 15 years.
She had worked all time at an employment office using a mobile phone
provided by her employer as a working tool for about half time of the
daily work. She used no protective measurements like a hands-free
device or loudspeaker, and used the handheld phone the whole time at
the same side of the brain where her PCNSL was diagnosed. About 50%
of energy absorbed in the brain is within the temporal lobe and about
10% is absorbed in the parieto-occipital lobes from mobile phones
marketed 2001 and later [11]. As seen in Fig. 2 her PCNSL developed in
the most radiated area of the brain.
Pesticides and persistent organic pollutants are known risk factors
for NHL, for overview see [12,13]. Some of these, like 2.3.7.8-tetra-
chlorodibenzo-p-dioxin (TCDD) and polychlorinated biphenyls (PCBs),
are immunosuppressive agents and an interaction with Epstein-Barr
virus (EBV) has been shown for the risk of NHL [13–15].
Biological aspects
Exposure of glioma cells for 2 h to 27 or 2,450 MHz continuous-
wave RF radiation in vitro modulated the rates of DNA and RNA
synthesis. The alterations indicated effects on cell proliferation and
were not caused by RF-induced cell heating. The dose response for ei-
ther frequency of the radiation was biphasic. Exposure to specific ab-
sorption rate (SAR) of 50 W/kg or less stimulated whereas higher SAR
suppressed DNA and RNA synthesis [16]).
Whole human blood was exposed or sham‐exposed in vitro for 2 h to
27 or 2,450 MHz RF radiation. Exposure to radiation at either fre-
quency at specific absorption rates below 50 W/kg resulted in a do-
se‐dependent, statistically significant increase of
3
H‐TdR uptake,
whereas exposure at 50 W/kg or higher suppressed
3
H‐TdR uptake re-
lative to that of sham‐exposed cells. The biphasic, dose‐dependent ef-
fects of the radiation on lymphocyte proliferation were not dependent
on heating [17].
Animal studies
Compared with 200 sham exposed rats a statistically significant
increased incidence of primary malignant diseases combined at all sites
(p = 0.005) was found in exposed rats in the study by Chou et al [18].
Among the malignancies found in exposed rats were malignant lym-
phoma and thyroid cancer. SAR ranged from 0.144 W/kg to 0.4 W/kg
depending on the rats’weight in this study on 200 rats exposed to
2,450 MHz pulsed RF radiation 21.5 h per day for 25 months. Thus,
SAR was low compared to the International Commission on Non-Io-
nizing Radiation Protection (ICNIRP) guideline on SAR 2 W/kg to the
brain for use of mobile phones [19].
In a study on mice carrying a lymphomagenic oncogene the lym-
phoma risk was statistically significantly higher in the exposed mice
than in the controls [20]. The study included one hundred mice that
were sham-exposed and 101 exposed for two 30-min periods per day for
up to 18 months to 900 MHz pulsed RF radiation with power densities
Fig. 1. CAT scan of the brain shows a large 50 × 20 × 30 mm right sided
tumour (dark area) with central necrosis located in the temporal, parietal and
occipital lobes. Note the 10 mm deviation of the midline to the left with
compression of the ventricular system. The small picture shows the lateral view
of the sectional image.
L. Hardell, et al. Medical Hypotheses 144 (2020) 110052
2

2.6–13 W/m
2
(SAR 0.008–4.2 W/kg, averaging 0.13–1.4 W/kg). These
results were not replicated [21], but the latter study was criticized for
using different study methods.
Mice were exposed to RF radiation; 0 (sham), 0.04, 0.4 and 2 W/kg
SAR, and numbers of tumors of the lungs and livers in exposed animals
were statistically significantly higher than in sham-exposed controls
including numbers of malignant lymphoma [22]. A tumor-promoting
effect by RF radiation was found at low to moderate levels (0.04 and
0.4 W/kg SAR), well below ICNIRP exposure limits for users of mobile
phones [22].
National Toxicology program (NTP) study
In female mice exposed to GSM modulated cell phone RF radiation
for 2 years there were increased incidences of malignant lymphoma in
all exposed groups compared to the controls [23]. The increase was
statistically significant in the 2.5 W/kg (p = 0.004) and 5 W/kg groups
(p = 0.035). In the CDMA modulated cell phone RF radiation for
2 years the lymphoma incidence increased in female mice in all exposed
groups compared to the controls, statistically significant in the 2.5 W/
kg group (p = 0.035).
No conclusive evidence of increased incidence of malignant lym-
phoma was reported in female rats in the NTP study [24];p
trend = 0.537 for GSM modulated cell phone RF radiation and p
trend = 0.339 for CDMA modulated cell phone RF radiation, see also a
commentary on the results [25].
Human studies
No epidemiological studies on risk factors for PCNSL exists to our
knowledge. Since it is a rare disease studies would be hampered by low
numbers of cases. Few studies exist on malignant lymphoma overall and
exposure to RF radiation. In a case-control study male and female
subjects aged 18–74 years living in Sweden were included during a
period from 1 December 1999 to 30 April 2002 [26]. Controls were
selected from the national population registry. Exposure to different
agents was assessed by questionnaire. In total, 910 (91%) cases and
1,016 (92%) controls participated.
NHL of the B-cell type was not associated with the use of cellular or
cordless telephones. Regarding T-cell NHL and > 5 year latency period,
the use of analogue cellular phones yielded: OR = 1.46, 95%
CI = 0.58–3.70, digital: OR = 1.92, 95%; CI = 0.77–4.80 and cordless
phones: OR = 2.47; 95% CI = 1.09–5.60.
The corresponding results for certain lymphoma, e.g. of the cuta-
neous and leukaemia T-cell types, were for analogue phones:
OR = 3.41, 95%; CI = 0.78–15.0, digital: OR = 6.12, 95%;
CI = 1.26–29.7 and cordless phones: OR = 5.48, 95%; CI = 1.26–23.9.
The results indicated an association between T-cell NHL and the use of
cellular and cordless telephones. The study was however based on low
numbers and must be interpreted with caution. Regarding B-cell NHL
no association was found [26].
A case-control study in USA used a questionnaire to assess cellular
telephone use in 551 NHL cases and 462 frequency-matched population
controls [27]. Compared to persons who had never used cellular tele-
phones, the risk was not increased among regular users, OR = 0.9, 95%
CI = 0.6–1.4. Among regular users compared to those who had never
used hand-held cellular telephones, the risk of NHL was not statistically
significantly associated with minutes per week, duration, cumulative
lifetime or year of first use, although NHL was non-significantly higher
in men who used cellular telephones for more than 8 years; OR = 2.4,
95% CI = 0.8–7.0. NHL not otherwise specified was statistically sig-
nificantly increased in men using mobile phone with ≥6 years dura-
tion, OR = 4.4, 95% CI = 1.3–14.6. Little evidence linked use of cel-
lular telephones with total, diffuse large B-cell lymphoma or follicular
NHL. No results were presented for T-cell lymphoma.
Fig. 2. CAT scan of the brain with superimposed RF field (GSM 900 MHz) from a mobile phone held close to the right ear. Colour scale to the left shows SAR in Watts
per kilogram (Om Gandhi with courtesy).
Table 1
Joinpoint regression analysis of age-standardized incidence rates per 100,000
in men, all ages, for NHL (ICD-7 codes 200 + 202) in the Swedish Cancer
Register during 1970–2017. Two joinpoints detected (1990, 2005).
Change/year (%) 95% CI
1970–2017* +1.66 +1.40, +1.91
−1970–1990** +3.40 +3.10, +3.70
−1990–2005** −0.18 −0.68, +0.31
−2005–2017** +1.10 +0.47, +1.73
*AAPC (Average Annual Percent Change); **APC (Annual Percent Change).
L. Hardell, et al. Medical Hypotheses 144 (2020) 110052
3

Incidence of NHL in the Swedish Cancer Register
In men the incidence of NHL increased sharply during 1970–1990
with APC + 3.40, 95% CI + 3.10, +3.70%. In women the highest
increase was seen during 1977–1988 with APC + 4.42%, 95%
CI + 3.30, +5.55%. Thus, these results are similar in both genders. The
high APC during these time periods may be explained by exposure to
certain pesticides and persistent organic pollutants that were banned
during the 1970′s[28]. Phenoxy herbicides (2,4,5-T) and chlorophenols
that have been associated with NHL risk were banned on the Swedish
market in 1977 and 1978, respectively [28]. Regulations of the use of
some toxic persistent organic substances in the 1970′s has resulted in
lower contamination of the food chain [29]. Thus, reduced exposure
due to regulations to certain toxic chemicals may explain the lower
increasing incidence during the last three decades.
The increasing incidence of NHL was lower in the last time period in
our study, although still statistically significant. The increase may
partly be explained by exposure to other chemical agents such as the
widely used herbicide glyphosate that has been indicated to increase
the NHL risk [30,31]. Immunological impairment is a contributing risk
factor to NHL. During the last three decades exposure to RF radiation
has increased substantially which may have some detrimental effects on
the immune system and thus contribute to the increasing incidence.
Thus, it cannot be excluded that RF radiation is a risk factor for NHL.
PCNSL is a rare disease and incidence data cannot be studied by using
the Swedish Cancer Register. Instead the Swedish Lymphoma Register
was used by Eloranta et al. [3].
RF radiation may suppress the immune system, for example through
the human Vitamin-D receptor and its ligand, which is reported to be
associated with many chronic inflammatory and autoimmune diseases
[32]. Other studies report that long lasting low exposure to RF radiation
in rats down to 2500 µW/m
2
and SAR-values as low as 600 µW/kg can
induce oxidative stress, with lowered antioxidant levels and increased
free radicals, an inflammatory response through increase in pro-in-
flammatory cytokines and DNA damage [33–35]. Of interest is a recent
article that stated: “In conclusion, 900-, 1800-, and 2100-MHz RFR
[radiofrequency radiation] emitted from mobile phones may cause oxidative
damage, induce increase in lipid peroxidation, and increase oxidative DNA
damage formation in the frontal lobe of the rat brain tissues. Furthermore,
2100-MHz RFR may cause formation of DNA single-strand breaks.”[36].
Thus, immunological impairment and oxidative damage from RF ra-
diation may be of etiologic importance in NHL.
RF radiation from GSM 915 MHz and UMTS 1,947 MHz on human
lymphocytes showed a long-lasting inhibition of DNA repair foci. The
Fig. 3. Joinpoint regression analysis of age-standardized incidence rates per 100,000 in men, all ages, for NHL (ICD-7 codes 200 + 202) in the Swedish Cancer
Register during 1970–2017. (https://sdb.socialstyrelsen.se/if_can/val.aspx).
Table 2
Joinpoint regression analysis of age-standardized incidence rates per 100,000
in women, all ages, for NHL (ICD-7 codes 200 + 202) in the Swedish Cancer
Register during 1970–2017. Two joinpoints detected (1977, 1988).
Change/year (%) 95% CI
1970–2017* +1.31 +0.92, +1.70
−1970–1977** −0.11 −1.94, +1.75
−1977–1988** +4.42 +3.30, +5.55
−1988–2017** +0.49 +0.27, +0.71
*AAPC (Average Annual Percent Change); **APC (Annual Percent Change).
L. Hardell, et al. Medical Hypotheses 144 (2020) 110052
4

exposure from UMTS had the highest effect [37]. Mesenchymal stem
cells can be more sensible to RF radiation than differentiated cells and
the capacity to repair DNA double-strand breaks was more affected in
stem cells than in fibroblasts from humans [38].
A study on two groups of rats exposed to 1.4 mW/cm
2
RF radiation
1,800 MHz from a mobile phone base station positioned 8 m away for
5 weeks showed an increase in white blood cell counts where the
lymphocytes increased 50–100% and the neutrophíls decreased about
40% compared to a control group [39].
Three studies from India on people living near mobile phone base
stations compared to people living further away showed a higher fre-
quency of micronuclei, induced DNA damage and lowering of anti-
oxidant levels in blood lymphocytes [40–42]. DNA unrepaired damage
may lead to genomic instability and in the long run induction of cancer
[40].
Conclusions
No etiologic factor has clearly been defined to explain the increasing
incidence of brain lymphoma. However, it has occurred during a time
period when RF radiation to the brain from wireless phones has in-
creased. Based on human epidemiology studies and laboratory studies
there is evidence that malignant lymphoma may be related to exposure
to RF radiation. This case-report stimulates the hypothesis that the in-
creasing incidence of PCNSL may be caused by exposure to RF fields.
The effects from RF radiation through DNA damage and decreased
DNA repair, by oxidative stress in the cells and increase in pro-in-
flammatory cytokines are some possible pathways that may influence
the immune system and the lymphocytes. RF radiation from a mobile
phone hold near the right ear during 4 h per working day during
15 years may have had an impact on the development of the PCNSL in
this female case report.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgement
Not applicable.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Ethics approval and consent to participate
The study was approved by the ethics committee: Regional Ethics
Committee, Uppsala University; Uppsala, Sweden. DNR 2005:367.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
Fig. 4. Joinpoint regression analysis of age-standardized incidence rates per 100,000 in women, all ages, for NHL (ICD-7 codes 200 + 202) in the Swedish Cancer
Register during 1970–2017. (https://sdb.socialstyrelsen.se/if_can/val.aspx).
L. Hardell, et al. Medical Hypotheses 144 (2020) 110052
5

doi.org/10.1016/j.mehy.2020.110052.
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