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International Journal of
Environmental Research
and Public Health
Article
Is the Increasing Incidence of Thyroid Cancer in the
Nordic Countries Caused by Use of Mobile Phones?
Michael Carlberg 1, *, Tarmo Koppel 2, Lena K. Hedendahl 1and Lennart Hardell 1
1The Environment and Cancer Research Foundation, Studievägen 35, SE 702 17 Örebro, Sweden;
lenahedendahl@telia.com (L.K.H.); lennart.hardell@environmentandcancer.com (L.H.)
2School of Business and Governance, Tallinn University of Technology, SOC353 Ehitajate Tee 5,
19086 Tallinn, Estonia; tarmo.koppel@taltech.ee
*Correspondence: michael.carlberg@environmentandcancer.com
Received: 29 October 2020; Accepted: 5 December 2020; Published: 7 December 2020
Abstract:
The International Agency for Research on Cancer (IARC) at the World Health Organization
(WHO) categorized in 2011 radiofrequency (RF) as a possible human carcinogen, Group 2B. During use
of the handheld wireless phone, especially the smartphone, the thyroid gland is a target organ.
During the 21st century, the incidence of thyroid cancer is increasing in many countries. We used the
Swedish Cancer Register to study trends from 1970 to 2017. During that time period, the incidence
increased statistically significantly in women with average annual percentage change (AAPC) +2.13%,
95% confidence interval (CI) +1.43, +2.83%. The increase was especially pronounced during 2010–2017
with annual percentage change (APC) +9.65%, 95% CI +6.68, +12.71%. In men, AAPC increased
during 1970–2017 with +1.49%, 95% CI +0.71, +2.28%. Highest increase was found for the time
period 2001–2017 with APC +5.26%, 95% CI +4.05, +6.49%. Similar results were found for all Nordic
countries based on NORDCAN 1970–2016 with APC +5.83%, 95% CI +4.56, +7.12 in women from
2006 to 2016 and APC +5.48%, 95% CI +3.92, +7.06% in men from 2005 to 2016. According to the
Swedish Cancer Register, the increasing incidence was similar for tumors
≤
4 cm as for tumors >4 cm,
indicating that the increase cannot be explained by overdiagnosis. These results are in agreement with
recent results on increased thyroid cancer risk associated with the use of mobile phones. We postulate
that RF radiation is a causative factor for the increasing thyroid cancer incidence.
Keywords:
mobile phone; cordless phone; thyroid cancer; Swedish Cancer Register; NORDCAN;
radiofrequency electromagnetic fields; RF-EMF; ionizing radiation; incidence; Nordic countries
1. Introduction
One established risk factor for thyroid cancer, especially of the papillary type, is ionizing
radiation [
1
]. The first reports of an increased risk were published in the late 1940s and early 1950s [
2
,
3
].
Since then, studies have associated thyroid cancer with diagnostic x-ray investigation [
2
], external
radiotherapy [
4
], and nuclear fallout after the use of A-bombs in Hiroshima and Nagasaki [
5
] as well as
after the Chernobyl and Fukushima disasters [
6
]. In Belarus, fallout of radioiodine after the Chernobyl
accident has been associated with increased incidence of thyroid cancer in children and adolescents [
7
].
No clear excess to thyroid cancer related to caesium-137 deposition was found in Sweden [8].
Thyroid cancer is more common in women than in men. Hormonal and reproductive factors may
explain that difference [9,10].
During the last two decades, a striking increase in the incidence has been reported in the Nordic
countries [
11
]. Use of computed tomography (CT) and positron emission tomography–computed
tomography (PET-CT) for diagnostic procedures may have contributed to the increased incidence,
but does not seem to explain the whole increase [12,13].
Int. J. Environ. Res. Public Health 2020,17, 9129; doi:10.3390/ijerph17239129 www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2020,17, 9129 2 of 9
The thyroid is exposed to radiofrequency (RF) radiation during use of mobile and cordless (DECT)
phones [
14
]. This is especially the situation for smartphones that have been increasingly used since the
early 2000s. In our previous study, we postulated that exposure to RF-radiation might be a causative
factor for the increasing incidence [11].
A case-control study on mobile phone use suggested an increased risk for thyroid cancer [
15
].
The same material was used to study genotype–environment interaction between single nucleotide
polymorphism (SNPs) and mobile phone use [
16
]. The study showed that mobile phone use increased
the risk for thyroid cancer when genetic variants were present within some genes. It was concluded
that pathways related to DNA repair may be involved in the increased risk for thyroid cancer associated
with mobile phone use. The increased risk was seen regardless of tumor size,
≤
10 mm versus >10 mm,
or latency, ≤13 years versus >13 years [16].
The U.S. National Toxicology Program (NTP) results on the toxicology and carcinogenicity of RF
radiation in rats and mice showed no increased thyroid cancer incidence in mice [
17
]. A statistically
significant increased incidence of C cell hyperplasia was found in the two years of GSM exposed
groups (1.5, 3, and 6 W/kg, respectively) of female rats [
18
]. In males, a statistically non-significant
increased incidence was observed in the 1.5 W/kg exposure group. C cell hyperplasia is a precursor to
familial medullary thyroid cancer in humans and may also be a precursor to other types of thyroid
cancer [19].
We studied the incidence of thyroid cancer using the Swedish Cancer Register and NORDCAN
for the Nordic countries. Our previous published results [
11
] were thus updated. Since no personal
identification was used, no ethical permission was needed.
2. Materials and Methods
2.1. Study Design
The National Board of Health and Welfare administers the Swedish Cancer Register. It has
yearly updates and was started in 1958. The tumor diagnosis is based on clinical examination,
histology/cytology, surgery, and/or autopsy. Additionally, laboratory investigations, CT, and MRI are
used for diagnosis.
The ICD-7 code 194 is used in the Swedish Cancer Register for thyroid cancer. We studied the
aged-adjusted incidence per 100,000 person years according to the world population for the time
period 1970–2017. The database was updated until 2018, but the last year was excluded due to a
delay in the reporting of cases leading to an underestimation of number of tumors for that year
according to the Swedish Cancer Register (note in the online database). The data are available online
(https://sdb.socialstyrelsen.se/if_can/val.aspx).
NORDCAN was used for all Nordic countries (Sweden, Denmark, Finland, Norway, and Iceland)
to study thyroid cancer incidence (ICD-10 code C73) for the time period 1970–2016 (latest update).
Thereby age-adjustment was made according to the world population. The data are available online
(http://www-dep.iarc.fr/NORDCAN/english/frame.asp).
2.2. Statistical Methods
Trends in age-standardized incidence of thyroid cancer by fitting a model of 0–5 joinpoints settings
in default mode was analyzed using the
National Cancer Institute (NCI) Joinpoint Regression Analysis program, version 4.8.0.1 [
20
].
Annual percentage changes (APC) and 95% confidence intervals (CI) were calculated for each linear
segment when joinpoints were detected. For the whole time period, average annual percentage
changes (AAPC) were calculated using the average of the APCs weighted by the length of the segment.
To calculate APC and AAPC, the data were log-transformed prior to analysis. Thus, it was not possible
to perform joinpoint regression analysis when there were years with no cases during the time period.
Int. J. Environ. Res. Public Health 2020,17, 9129 3 of 9
3. Results
3.1. The Swedish Cancer Register
For the whole study period of 1970–2017, the incidence increased statistically significantly in
women with AAPC +2.13% (95% CI +1.43, +2.83%), Table 1. Three joinpoints were detected, 1979,
1999, and 2010 with especially high APC for the last period 2010–2017; APC +9.65% (95% CI +6.68,
+12.71%). AAPC was statistically significantly increased in all age groups except for the oldest age of
80+years. It is to be noted that AAPC also increased statistically significantly among the youngest
persons of 0–19 years with +1.69% (95% CI +0.88, +2.51%).
Figure 1shows the increasing incidence in women from 1999. Note, especially from 2010, a steep
increasing curve.
Int. J. Environ. Res. Public Health 2020, 17, x 3 of 10
3. Results
3.1. The Swedish Cancer Register
For the whole study period of 1970–2017, the incidence increased statistically significantly in
women with AAPC +2.13% (95% CI +1.43, +2.83%), Table 1. Three joinpoints were detected, 1979,
1999, and 2010 with especially high APC for the last period 2010–2017; APC +9.65% (95% CI +6.68,
+12.71%). AAPC was statistically significantly increased in all age groups except for the oldest age of
80+ years. It is to be noted that AAPC also increased statistically significantly among the youngest
persons of 0–19 years with +1.69% (95% CI +0.88, +2.51%).
Figure 1 shows the increasing incidence in women from 1999. Note, especially from 2010, a steep
increasing curve.
Figure 1. Joinpoint regression analysis of age-standardized incidence of thyroid cancer for women,
all ages 1970–2017. Incidence per 100,000 inhabitants for ICD-7 code 194 according to the Swedish
Cancer Register (https://sdb.socialstyrelsen.se/if_can/val.aspx).
According to Table 2, the increasing incidence of thyroid cancer was less dramatic in men during
1970–2017 with AAPC +1.49% (95% CI +0.71, +2.28%). AAPC increased statistically significantly in all
age groups except for 80+ years. Due to few persons in the youngest age group 0–19 years (n = 98),
AAPC could not be calculated. The highest increasing APC was found in men aged 20–39 years for
the time period 2001–2017; +7.80%, (95% CI +4.17, 11.54%).
Figure 1.
Joinpoint regression analysis of age-standardized incidence of thyroid cancer for women,
all ages 1970–2017. Incidence per 100,000 inhabitants for ICD-7 code 194 according to the Swedish
Cancer Register (https://sdb.socialstyrelsen.se/if_can/val.aspx).
Int. J. Environ. Res. Public Health 2020,17, 9129 4 of 9
Table 1.
Joinpoint regression analysis of thyroid cancer incidence in women in the Swedish Cancer
Register 1970–2017. ICD-7 code 194 (https://sdb.socialstyrelsen.se/if_can/val.aspx). APC =Annual
Percentage Change (APC 1 =time from 1970 to first joinpoint; APC 2 =time from first joinpoint to 2017
or to second joinpoint; APC 3 =time from second joinpoint to 2017 or to third joinpoint; APC 4 =time
from third joinpoint to 2017); AAPC =Average Annual Percentage Change.
ICD-7 Joinpoint
Location
APC 1
(95% CI)
APC 2
(95% CI)
APC 3
(95% CI)
APC 4
(95% CI)
AAPC
(95% CI)
194
All women
(n=13,020)
1979; 1999;
2010
+2.26
(+0.36,
+4.20)
−1.50
(−2.10,
−0.90)
+4.13
(+2.48,
+5.81)
+9.65
(+6.68,
+12.71)
+2.13
(+1.43,
+2.83)
0–19 years
(n=318)
No joinpoint
detected - - - -
+1.69
(+0.88,
+2.51)
20–39 years
(n=2935) 2002
+0.53
(+0.07,
+0.99)
+7.16
(+5.64,
+8.70)
- -
+2.60
(+2.05,
+3.15)
40–59 years
(n=4223) 2002
−0.95
(−1.60,
−0.29)
+7.39
(+5.20,
+9.63)
– -
+1.64
(+0.85,
+2.43)
60–79 years
(n=4166) 1974; 2003
+9.50
(−2.44,
+22.91)
−2.11
(−2.70,
−1.52)
+6.00
(+4.20,
+7.83)
-
+1.20
(+0.06,
+2.35)
80+years
(n=1378) 1979; 1996
+2.40
(−1.75,
+6.73)
−4.57
(−6.22,
−2.90)
+0.52
(−0.63,
+1.69)
-
−1.00
(−2.08,
+0.10)
According to Table 2, the increasing incidence of thyroid cancer was less dramatic in men during
1970–2017 with AAPC +1.49% (95% CI +0.71, +2.28%). AAPC increased statistically significantly in all
age groups except for 80+years. Due to few persons in the youngest age group 0–19 years (n=98),
AAPC could not be calculated. The highest increasing APC was found in men aged 20–39 years for the
time period 2001–2017; +7.80%, (95% CI +4.17, 11.54%).
Int. J. Environ. Res. Public Health 2020, 17, x 4 of 10
The age-standardized incidence of thyroid cancer (ICD-194) per 100,000 using joinpoint
regression analysis is shown in Figure 2. In men, an increasing incidence is shown from 2001.
Figure 2. Joinpoint regression analysis of age-standardized incidence of thyroid cancer for men, all
ages 1970–2017. Incidence per 100,000 inhabitants for ICD-7 code 194 according to the Swedish Cancer
Register (https://sdb.socialstyrelsen.se/if_can/val.aspx).
Table 1. Joinpoint regression analysis of thyroid cancer incidence in women in the Swedish Cancer
Register 1970–2017. ICD-7 code 194 (https://sdb.socialstyrelsen.se/if_can/val.aspx). APC = Annual
Percentage Change (APC 1 = time from 1970 to first joinpoint; APC 2 = time from first joinpoint to
2017 or to second joinpoint; APC 3 = time from second joinpoint to 2017 or to third joinpoint; APC 4
= time from third joinpoint to 2017); AAPC = Average Annual Percentage Change.
ICD-7 Joinpoint Location APC 1
(95% CI)
APC 2
(95% CI)
APC 3
(95% CI)
APC 4
(95% CI)
AAPC
(95% CI)
194
All women
(n = 13,020) 1979; 1999; 2010 +2.26
(+0.36, +4.20)
−1.50
(−2.10, −0.90)
+4.13
(+2.48, +5.81)
+9.65
(+6.68, +12.71)
+2.13
(+1.43, +2.83)
0–19 years
(n = 318) No joinpoint detected - - - - +1.69
(+0.88, +2.51)
20–39 years
(n = 2935) 2002 +0.53
(+0.07, +0.99)
+7.16
(+5.64, +8.70) - -
+2.60
(+2.05, +3.15)
40–59 years
(n = 4223) 2002 −0.95
(−1.60, −0.29)
+7.39
(+5.20, +9.63) -- -
+1.64
(+0.85, +2.43)
60–79 years
(n = 4166) 1974; 2003 +9.50
(−2.44, +22.91)
−2.11
(−2.70, −1.52)
+6.00
(+4.20, +7.83) - +1.20
(+0.06, +2.35)
80+ years
(n = 1378) 1979; 1996 +2.40
(−1.75, +6.73)
−4.57
(−6.22, −2.90)
+0.52
(−0.63, +1.69) - −1.00
(−2.08, +0.10)
Figure 2.
Joinpoint regression analysis of age-standardized incidence of thyroid cancer for men, all ages
1970–2017. Incidence per 100,000 inhabitants for ICD-7 code 194 according to the Swedish Cancer
Register (https://sdb.socialstyrelsen.se/if_can/val.aspx).
Int. J. Environ. Res. Public Health 2020,17, 9129 5 of 9
Table 2.
Joinpoint regression analysis of thyroid cancer incidence in men in the Swedish Cancer Register
1970–2017. ICD-7 code 194 (https://sdb.socialstyrelsen.se/if_can/val.aspx). APC =Annual Percentage
Change (APC 1 =time from 1970 to first joinpoint; APC 2 =time from first joinpoint to 2017 or to second
joinpoint; APC 3 =time from second joinpoint to 2017); AAPC =Average Annual Percentage Change.
ICD-7 Joinpoint
Location
APC 1
(95% CI)
APC 2
(95% CI)
APC 3
(95% CI)
AAPC
(95% CI)
194
All men
(n=5047) 1977; 2001 +3.31
(−0.78, +7.56)
−1.45
(−2.11, −0.79)
+5.26
(+4.05, +6.49)
+1.49
(+0.71, +2.28)
0–19 years
(n=98) -----
20–39 years
(n=800) 2001 −0.67
(−1.92, +0.60)
+7.80
(+4.17, +11.54) -+2.13
(+0.72, +3.57)
40–59 years
(n=1508) 2003 −0.58
(-1.25, +0.09)
+5.54
(+2.99, +8.16) -+1.21
(+0.36, +2.06)
60–79 years
(n=2184) 1980; 2001 +2.69
(−0.10, +5.56)
−2.52
(−3.46, −1.57)
+4.77
(+3.36, +6.20)
+1.02
(+0.17, +1.87)
80+years
(n=457)
No joinpoint
detected - - - −1.45
(−2.64, −0.24)
3.2. NORDCAN
In women, based on NORDCAN, the incidence of thyroid cancer increased statistically significantly
during 1970–2016 with AAPC +2.18% (95% CI +1.73, +2.64%), Table 3.
Table 3.
Joinpoint regression analysis of thyroid cancer incidence in women and men in the Nordic
countries according to NORDCAN 1970–2016, ICD-10 code C73 (https://www-dep.iarc.fr/NORDCAN/
english/frame.asp). APC =Annual Percentage Change (APC 1 =time from 1970 to first joinpoint;
APC 2 =time from first joinpoint to 2016 or to second joinpoint; APC 3 =time from second joinpoint to
2016); AAPC =Average Annual Percentage Change.
ICD-10 Joinpoint
Location
APC 1
(95% CI)
APC 2
(95% CI)
APC 3
(95% CI)
AAPC
(95% CI)
C73
All women (n=36,050)
1976; 2006 +4.61
(+1.90, +7.39)
+0.52
(+0.28, +0.77)
+5.83
(+4.56, +7.12)
+2.18
(+1.73, +2.64)
All men (n=13,078) 2005 +0.35
(+0.09, +0.61)
+5.48
(+3.92, +7.06) -+1.55
(+1.15, +1.96)
This was based on 36,050 female cancer cases. Two joinpoints were found: 1976 and 2006.
During 2006 to 2016, APC increased statistically significantly with +5.83% (95% CI +4.56, +7.12%).
These results are also shown in Figure 3.
The incidence increased statistically significantly in men during 1970–2016 with AAPC +1.55%
(95% CI +1.15, +1.96%), Table 3. Highest increase was found during more recent years with joinpoint
2005; APC +5.48% (95% CI +3.92, +7.06%), see also Figure 4.
Int. J. Environ. Res. Public Health 2020,17, 9129 6 of 9
Int. J. Environ. Res. Public Health 2020, 17, x 6 of 10
Figure 3. Joinpoint regression analysis of age-standardized incidence of thyroid cancer for women,
all ages 1970–2016. Incidence per 100,000 inhabitants for ICD-10 code C73 in the Nordic countries
according to NORDCAN (https://www-dep.iarc.fr/NORDCAN/english/frame.asp).
Figure 4. Joinpoint regression analysis of age-standardized incidence of thyroid cancer for men, all
ages 1970–2016. Incidence per 100,000 inhabitants for ICD-10 code C73 in the Nordic countries
according to NORDCAN (https://www-dep.iarc.fr/NORDCAN/english/frame.asp).
Figure 3.
Joinpoint regression analysis of age-standardized incidence of thyroid cancer for women,
all ages 1970–2016. Incidence per 100,000 inhabitants for ICD-10 code C73 in the Nordic countries
according to NORDCAN (https://www-dep.iarc.fr/NORDCAN/english/frame.asp).
Int. J. Environ. Res. Public Health 2020, 17, x 6 of 10
Figure 3. Joinpoint regression analysis of age-standardized incidence of thyroid cancer for women,
all ages 1970–2016. Incidence per 100,000 inhabitants for ICD-10 code C73 in the Nordic countries
according to NORDCAN (https://www-dep.iarc.fr/NORDCAN/english/frame.asp).
Figure 4. Joinpoint regression analysis of age-standardized incidence of thyroid cancer for men, all
ages 1970–2016. Incidence per 100,000 inhabitants for ICD-10 code C73 in the Nordic countries
according to NORDCAN (https://www-dep.iarc.fr/NORDCAN/english/frame.asp).
Figure 4.
Joinpoint regression analysis of age-standardized incidence of thyroid cancer for men, all ages
1970–2016. Incidence per 100,000 inhabitants for ICD-10 code C73 in the Nordic countries according to
NORDCAN (https://www-dep.iarc.fr/NORDCAN/english/frame.asp).
Int. J. Environ. Res. Public Health 2020,17, 9129 7 of 9
4. Discussion
The main result in this study was increasing thyroid cancer incidence in Sweden during
the study period 1970–2017, especially during the more recent years in both men and women.
The increase was even higher than during 1970–2013, as presented in our previous publication [
11
].
Thus, AAPC in women was now +2.13% compared with +1.19% during our previous study period.
The corresponding results in men were +1.49% and +0.77%, respectively. In men, the AAPC increase
was now statistically significant.
Increasing statistically significant AAPC was found in all age groups for both genders except those
aged 80+years and in men 0–19 years. These results were based on lower numbers and are similar to
those in our previous publication [
11
]. In both men and women, increasing APC was found from early
2000. Thus, since 2002, thyroid cancer incidence increased in women yearly more than +7% in the
age groups 20–39 and 40–59 years. From 2003, APC increased with +6% in the age group 60–79 years.
It is noteworthy that for all women, the yearly increase was almost +10% during 2010–2017. A similar
pattern was found in men with APC about +5% to almost +8% in the three age groups 20–79 years
since the beginning of the 21st century.
According to NORDCAN, the thyroid cancer incidences increased statistically significantly from
2006 in women and from 2005 in men based on a fairly large number of cancer cases. The increase was
comparable in both women and men during these time periods at +5.83% versus +5.48%.
Since this is a register-based study, the results must be interpreted with caution. The results
were given for age groups and were gender-specific. However, these results do definitely indicate an
etiologic impact of an exogenous cancer-causing factor with increasing exposure over time. In our
previous publication [
11
], we made a comprehensive discussion of different risk factors. One risk factor
might be pollution [
21
]. Another good candidate is no doubt the use of wireless phones, especially
the handheld smartphone that due to the antenna position gives RF exposure to the thyroid gland.
This organ is one of the highest exposed aside from the brain during the use of smartphones [
14
].
These phones have been increasingly common since the early 21st century and are now the only types
that are marketed. The first generations of mobile phones were introduced in the 1980s as well as the
cordless desktop phone (DECT). Additionally, these handheld phones give offRF radiation to the head
and neck region.
A fairly short latency period has been found for ionizing radiation induced thyroid cancer with
increasing risk beginning 5–10 years after radiation [
22
]. Thus, the sharp current increase in thyroid
cancer incidence may be radiation induced, most likely RF radiation from the handheld phone. It is
noteworthy that Luo et al. [16] also found increased risk in the shortest latency period of ≤13 years.
Increasing thyroid cancer incidence has been seen worldwide during the last 20 years, and is
expected to be the fourth most common cancer by 2030 [
23
]. The rising trend has been reported in
different continents with different health systems and ethnicities [24].
So called overdiagnosis has been suggested to explain the increasing thyroid cancer incidence [
12
]
due to better access to health care and screening. However, screening for thyroid cancer is not
performed in the Nordic countries and there are no social or demographic differences for health
access. Diagnostic patterns might be a contributing factor but do not explain the increasing incidence,
especially during recent years [
25
]. This is supported by the recent results also showing increased risk
from RF radiation for tumors
≤
10 mm [
16
]. Interestingly, according to the Swedish Cancer Register,
there is a similar incidence increase during 2005–2018 for tumors
≤
4 cm (T1-T2) as for tumors >4 cm
(T3-T4), or with invasive growth into surrounding tissue. The percentage between these groups was
about the same over the years, indicating that the increasing incidence is not due to overdiagnosis [
26
].
Ionizing radiation is an established risk factor. Increasing use of x-ray investigations for diagnostic
procedures may be contributing to the increased incidence, especially for the radio-sensitive papillary
type [
27
]. Chest CT and whole-body trauma CT are increasingly used, but does not explain the
pattern of increasing incidence of thyroid cancer; for discussion, see Carlberg et al. [
11
]. Diet has been
suggested to be of etiologic importance for thyroid cancer. In a prospective study, intake of iodine-rich
Int. J. Environ. Res. Public Health 2020,17, 9129 8 of 9
foods and goitrogens were indicated to influence the risk [
28
]. However, there have been no known
sudden changes of the food habits in the Nordic countries that can explain our findings.
5. Conclusions
Thyroid cancer incidence has been steeply increasing in Sweden and all Nordic countries during
the 21st century. Use of the handheld mobile phone is increasing, in particular, the smartphone gives
high RF radiation exposure to the thyroid gland. It is postulated that this might be a causative factor
for the increasing incidence supported by human epidemiology that has shown an association between
mobile phone use and thyroid cancer.
Author Contributions:
Conceptualization, L.H. and M.C.; Methodology, L.H. and M.C.; Software, M.C.; Formal
analysis, M.C.; Investigation, L.H., M.C., T.K., and L.K.H.; Data curation, M.C.; Writing—original draft preparation,
L.H.; Writing—review and editing, L.H., M.C., T.K., and L.K.H.; Supervision, L.H. All authors have read and
agreed to the published version of the manuscript.
Funding: This research received no external funding.
Conflicts of Interest: The authors declare no conflict of interest.
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