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Acute effects of 30 minutes of exposure to a smartphone call on in vitro platelet function

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Background. Significant concerns are now regularly raised about the safety of excessive mobile phone use. This study was aimed to assess the acute effects of radiofrequency waves emitted by a commercial smartphone on platelet function. Materials and methods. Two sequential citrated blood samples were collected from 16 healthy volunteers recruited from laboratory staff. The first sample was placed in a plastic rack, 1 cm distant from a commercial smartphone receiving a 30-min call and emitting 900 MHz radiofrequency waves. The second sample was placed in another plastic rack, isolated from radiofrequency wave sources, for the same period. The platelet count and the mean platelet volume were then assessed in all blood samples, whereas platelet function was evaluated using the platelet function analyser-100 (PFA-100). Results. A 30-min exposure of citrated blood to smartphone radiofrequency waves induced significant prolongation of collagen-epinephrine aggregation (median increase, 10%) and a considerable increase of mean platelet volume (median increase, 5%), whereas collagen-adenosine diphosphate aggregation and platelet count remained unchanged. Discussion. This study demonstrates that smartphone radiofrequency waves induce significant perturbation of platelet structure and function, thus providing further support to concerns regarding excessive use of mobile phones. Caution should also be taken with regards to blood products containing platelets, which should be kept far away from mobile phones and smartphones throughout the production pipeline and storage period.
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Blood Transfus DOI 10.2450/2016.0327-15
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Acute effects of 30 minutes of exposure to a smartphone call
on  platelet function
Giuseppe Lippi, Elisa Danese, Giorgio Brocco, Matteo Gelati, Gian Luca Salvagno, Martina Montagnana
Section of Clinical Biochemistry, University of Verona, Verona, Italy
Background. Significant concerns are now regularly raised about the safety of excessive mobile
phone use. This study was aimed to assess the acute effects of radiofrequency waves emitted by a
commercial smartphone on platelet function.
Materials and methods. Two sequential citrated blood samples were collected from 16 healthy
volunteers recruited from laboratory staff. The first sample was placed in a plastic rack, 1 cm distant
from a commercial smartphone receiving a 30-min call and emitting 900 MHz radiofrequency waves.
The second sample was placed in another plastic rack, isolated from radiofrequency wave sources,
for the same period. The platelet count and the mean platelet volume were then assessed in all blood
samples, whereas platelet function was evaluated using the platelet function analyser-100 (PFA-100).
Results. A 30-min exposure of citrated blood to smartphone radiofrequency waves induced
significant prolongation of collagen-epinephrine aggregation (median increase, 10%) and a
considerable increase of mean platelet volume (median increase, 5%), whereas collagen-adenosine
diphosphate aggregation and platelet count remained unchanged.
Discussion. This study demonstrates that smartphone radiofrequency waves induce significant
perturbation of platelet structure and function, thus providing further support to concerns regarding
excessive use of mobile phones. Caution should also be taken with regards to blood products
containing platelets, which should be kept far away from mobile phones and smartphones throughout
the production pipeline and storage period.
Keywords: mobile phone, radiofrequency, platelets, PFA-100.
Introduction
Since their commercial introduction in the late
1980s, the use of mobile phones and smartphones
has increased exponentially around the globe, with
an estimated 6.9 billion subscriptions in 2014
1
. Along
with an increasing number of users, the amount of time
spent using these devices has also risen considerably
1
.
Most mobile phones, including smartphones, generate
a form of electromagnetic, non-ionising energy that
is typically known as radiofrequency (RF) waves,
which lie between frequency modulation (FM) radio
waves and microwaves. More specifically, mobile
phones are low-powered RF transmitters that operate
at frequencies comprised between 450 and 2,700 MHz
and peak powers ranging between 0.1 and 2 Watts
1
.
Unlike microwave radiation, the lower energy
delivered by RF waves has long been considered
insufficient to increase body temperatures, and mobile
phones have, therefore, traditionally been believed to
be relatively safe. However, due to the ever growing
number of people using mobile phones and the longer
exposure periods, even a small increase in the risk
of adverse health effects may generate major public
health concerns. A former meta-analysis published in
2009, including 23 case-control studies and totalling
37,916 participants, concluded that the use of mobile
phones for 10 years or longer was associated with an
18% increased risk of tumours (odds ratio, 1.18; 95%
confidence interval [95% CI], 1.04-1.34)
2
. Two years
later, on behalf of the World Health Organization
(WHO) and the International Agency for Research
on Cancer (IARC), a Working Group of scientists
met in Lyon (France) to establish the potential
carcinogenic hazards attributable to exposure to
RF electromagnetic fields and deliberated that the
evidence, while still accumulating, is strong enough
to support the conclusion that the waves emitted
by mobile phones should be considered as possibly
carcinogenic to humans
3
. Interestingly, the WHO
has recently raised additional concerns about the
safety of mobile phone use, listing changes in brain
activity, reaction times and sleep pattern as potential
complications
1
. Additional epidemiological studies
have also shown that heavy use of mobile phones
may be associated with early spontaneous abortion
4
,
headache
5
, and hearing loss
6
.
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Lippi G at al
Blood Transfus DOI 10.2450/2016.0327-15
Of particular relevance to the current study,
platelets are small, non-nucleated blood elements
7
,
which play a crucial role in haemostasis, since they
contribute to generate the initial haemostatic plug that
helps to prevent acute bleeding upon blood vessel
injury, and also provide the physiological surface
for activation of coagulation factors, thus facilitating
ultimate stabilisation of the primary platelet plug
8
.
Platelet function is strongly influenced by a number of
environmental and behavioural conditions, including
body temperature
9,10
, nutrition
11
, air pollution
12
, exposure
to allergens
13
, and even sleep disturbances
14
. The aim of
this study was, therefore, to assess whether the RF waves
emitted by a commercial smartphone might generate
acute effects on platelet function in vitro.
Materials and methods
The study population consisted of 16 healthy
volunteers (mean age, 45±11 years, 13 females and 3
males), recruited from laboratory staff. None of the study
subjects had taken medications known to affect platelet
metabolism (i.e., antiplatelet or antihypertensive drugs)
during the week prior to the experiments. After drawing
two serum discard tubes (Vacutest Kima Srl, Padova,
Italy), two additional blood samples were collected
from an antecubital vein of the arm by a 0.8×38 mm,
21 gauge straight needle into a 13×75 mm, 3.5 mL
evacuated plastic tube containing 0.10
9
mol/L buffered
sodium citrate (Vacutest Kima Srl). All citrated blood
tubes were filled to the nominal volume and the various
steps of collection were standardised to identical resting
time of volunteers (i.e. 10 min) and identical time of
tourniquet placement (i.e. <30 s). All citrated blood tubes
were gently mixed by inversion six times immediately
after collection. The first citrated blood sample of each
volunteer was placed in a plastic rack, 1 cm distant
from the chassis of a commercial smartphone placed
in a horizontal position and powered by a 1,570 mAh
non-removable lithium battery. The characteristics of
the mobile phone are as follows: height, 12.4 cm; width,
5.9 cm; thickness 0.8 cm; carrier frequency, 900 MHz.
Immediately after the samples had been positioned in
the plastic rack, a call was placed on the smartphone
and the communication was manually activated for 30
min, with 3G and Wi-Fi connections disabled. During
this period, the rack with samples and smartphone was
gently inverted upside-down once every 5 min to prevent
sedimentation of corpuscular blood elements. After
the 30 min exposure to RF waves, the smartphone
was removed from the plastic rack and the samples
were left standing in an upright position for an
additional 60 min without further mixing. The second
citrated blood sample from each volunteer was placed
in another plastic rack for 90 min. In order to prevent
sedimentation of corpuscular blood elements, the
rack was gently inverted upside-down once every 5
min during the first 30 min period (as for the samples
exposed to smartphone RF waves). The samples were
then left in an upright position for the remaining 60 min,
without further mixing. The untreated blood samples
were carefully prevented from being in close contact
(<1 m) with mobile phones or other RF wave sources
throughout the study period.
The platelet count and the mean platelet volume
(MPV) were assessed in all blood samples using an Advia
2120 (Siemens Healthcare Diagnostics, Tarrytown, NY,
USA). Platelet function was then evaluated in whole
blood specimens using a platelet function analyzer-100
(PFA-100; Siemens Healthcare Diagnostics). In brief, this
instrument is equipped with two disposable cartridges
containing an internal active membrane coated with
collagen and adenosine diphosphate (C-ADP) or with
collagen and epinephrine (C-EPI). The contact of citrate
anticoagulated blood with the agonists under a high
shear condition triggers platelet activation and generates
a platelet plug that interrupts blood flow through the
capillary within the cartridge. The sample response is
finally reported as complete obstruction of the aperture,
and expressed as closure time (CT)
15
. The local reference
ranges are <116 s for C-ADP and <164 s for C-EPI,
respectively. The total imprecision of both tests has been
reported to be 5.5% for C-EPI and 4.3% for C-ADP
16
.
The same instrument and reagent lot were used during the
study, and all measurements were concluded within 4 h
after sample collection. The test results are expressed as
medians with interquartile ranges (IQR). The significance
of difference between untreated samples and those
exposed to the smartphone RF waves was assessed with
the Mann-Whitney-Wilcoxon test for paired samples,
using Analyse-it (Analyse-it Software Ltd, Leeds, UK).
The level of statistical significance was set at p<0.05.
Each volunteer provided informed consent to enrolment
in the study, which was carried out in accordance with the
Declaration of Helsinki and under the terms of relevant
local legislation.
Results
The main results of this study are shown in Table I.
The 30-min exposure of citrated blood to mobile phone
RF waves induced a highly significant prolongation
of C-EPI (median increase, 10%; IQR, 6-27%) and a
considerable increase of platelet size (median increase,
5%; IQR, 4-6%), whereas C-ADP and platelet count
remained substantially unchanged. Interestingly, a
prolongation of closure time was observed in 8/16
subjects for C-ADP (50%) and 15/16 subjects for C-EPI
(94%) (Figure 1). An increase of MPV was observed in
14/16 subjects (88%) (Figure 1).
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Blood Transfus DOI 10.2450/2016.0327-15
Acute effects of a smartphone on platelet function
Discussion
Mobile phones, including the increasingly popular
smartphones, emit a non-ionising electromagnetic
radiation that can be directly absorbed by human
cells and tissues located close to the source. On the
basis of this biological evidence, concerns have been
raised that excessive use of mobile phones (e.g., on
a daily basis and/or for long periods of time) may be
associated with health hazards due to the continuous
accumulation of potential RF wave-related damage.
For example, the potential association between use of
mobile phones and cancer has been the matter of a fierce
debate in recent decades. Although the level of evidence
remains insufficient for meaningful conclusions to
be drawn, the WHO has recently affirmed that RF
electromagnetic fields are potentially carcinogenic to
humans, so their use should be limited
1
. Additional
health concerns have been raised, besides the risk of
cancer, but little information has been published about
the potential effects of exposure to RF waves generated
by smartphones on platelet biology.
Coskun and Comlekci carried out an experimental
study including 16 healthy male Wistar rats, eight of
which were exposed to a pulsed electric field (PEF)
for 1 h a day for 10 consecutive days, whereas the
remaining eight rats were not exposed to the PEF
17
. The
platelet count of the rats exposed to the PEF increased
significantly (i.e., from 536 to 627×10
9
/L; p<0.05)
compared to that of the control animals. In another
experimental study, El-Bediwi et al. divided 50 healthy
Wistar rats into three groups: controls animals kept away
from RF fields (n=10) and rats constantly exposed to
900 MHz continuous RF fields for 1 h daily, 7 days
a week, for 3 months (n=20) or 6 months (n=20)
18
. A
substantial difference was noticed in the animals' platelet
counts, with the lowest values observed in rats constantly
exposed to RF fields for 6 months (−44% compared to
control rats). Interesting findings also emerged from a
recent study which explored platelet biology in vitro
after exposure to electromagnetic radiation
19
. In brief,
exposure of a suspension of platelets for 30 min to
electromagnetic radiation emitted by car electronics
60
70
80
90
100
110
120
130
140
150
C-ADP untreated C-ADP RF
Closure time (s)
80
90
100
110
120
130
140
150
160
170
180
190
200
210
C-EPI untreated C-EPI RF
Closure time (s)
7.0
7.5
8.0
8.5
9.0
9.5
10.0
MPV un treated MPV RF
Mean platelet volum e (fL)
Figure 1 - Acute effects of 30-min exposure to radiofrequency
waves from a commercial smartphone on in vitro
platelet function assessed by platelet aggregation
triggered by collagen and ADP (C-ADP) (top) or
collagen and epinephrine (C-EPI) (middle) and
mean platelet volume (MPV) (bottom).
RF: radiofrequency.
Table I - Acute effects of 30-min exposure to RF from
a commercial smartphone on in vitro platelet
function.
Parameter Untreated 30-min RF waves p
C-ADP (s) 97 (80-105) 96 (82-111) 0.264
C-EPI (s) 121 (103-137) 141 (124-161) <0.001
Platelets (x109/L) 281 (222-295) 282 (216-304) 0.144
MPV (fL) 7.8 (7.4-8.0) 8.1 (7.7-9.0) <0.001
C-ADP: collagen and ADP; C-EPI: collagen and epinephrine; MPV: mean
platelet volume; RF: radiofrequency.
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Lippi G at al
Blood Transfus DOI 10.2450/2016.0327-15
was associated with a 66% increase of catalase activity
and a 77% increase in malondialdehyde concentration.
Kozlovaite et al. measured platelet aggregation triggered
by either ADP or epinephrine before, immediately after
and 24 hours after RF ablation (500 kHz) in 39 patients
with cardiac arrhythmias
20
. Although a significant
reduction of platelet aggregation using both agonists
was observed immediately after RF ablation, the
decrease of platelet aggregation was more than double
using epinephrine than using ADP (i.e., 19% vs 8%).
Notably, the inhibition of platelet aggregation was
completely reversed 24 hours after RF ablation. The
influence of RF waves on platelet function was also
investigated by Wang et al., who exposed conventional
transfusion storage bags containing apheresed platelets
to continuous scanning for 5 consecutive days by means
of a RF identification (RFID) portal reader operating
at 915 MHz, and placed 35 to 55 cm away facing the
storage unit door
21
. Interestingly, the platelet aggregation
rate triggered by ADP remained substantially unvaried
in platelets subjected to continuous RFID scanning
compared to platelets not exposed to RFID scanning
throughout the study period.
Taken together, the results of our study show for
the first time that a 30 min exposure to a smartphone
call induces acute variations of both structure and
global function of human platelets, as mirrored by a
remarkable reduction of platelet aggregation/adhesion
triggered by C-EPI and a significant increase of platelet
size. With regards to potential explanations, the former
phenomenon mimics the platelet dysfunction that is
typically observed in patients with mild hereditary
platelet disorders (e.g., storage pool disease)
22,23
, in
patients with moderate and severe von Willebrand's
disease
24
, in those taking aspirin and other non-steroidal
anti-inflammatory drugs
25
, but is also a hallmark of
"exhausted platelets", i.e., platelets that have become
hypo-responsive as a result of previous "activation"
26
.
The increase of platelet size observed in the vast
majority of blood samples exposed to smartphone RF
waves in this study may also be a consequence of an
"activation" response. Seconds after activation, platelets
undergo a shape change, increase in size, over-express
surface activation markers and are both metabolically
and enzymatically more active
27
. Merging present data
with previous findings it is, therefore, plausible that
platelet irradiation at conventional mobile phone RF
waves (i.e., 900 MHz) may trigger hyper-activation
and some release of dense body content, which is
reflected by a durable increase of platelet size, but is then
followed by a gradual decline of platelet sensitivity and
responsiveness to milder agonists such as epinephrine
(Figure 2). Thus, after cessation of exposure to the RF,
the MPV measured with a conventional haematological
analyser would remain significantly increased compared
to that of resting platelets, whereas the responsiveness
of these partially exhausted platelets would decrease
significantly
28,29
.
Conclusions
In conclusion, exposure to smartphone RF waves
seemingly induces significant perturbations of platelet
structure and global function in vitro, thus providing
further support to the caution raised by various
international groups, including the US Food and
Drug Administration statement that the use of mobile
phones and/or smartphones should be reserved for
shorter conversations or times when a landline phone
is not available, and that hands-free devices should be
preferred since they allow a longer distance to be placed
between the phone and the user
30
. However, additional
in vivo studies are needed to establish whether local
perturbations of platelet structure and biology induced
by RF waves would actually be reflected in any increased
risk of cerebral thrombosis and/or intracranial bleeding
during or after smartphone use. Beside the potential
clinical implications, the significant impact that RF
waves may produce on platelet function would require
that blood products containing platelets should be kept
far from mobile phones and smartphones throughout the
production pipeline and the storage period, to prevent
the risk of transfusing patients with exhausted platelets.
Authorship contributions
GL and GB conceived and designed the study;
ED, MM, GLS and MG acquired data and ran the
experiments; GL analysed the data, performed the
statistical analysis and drafted the manuscript; GB, ED
and MM interpreted the results and critically revised
the manuscript. All Authors read and approved the final
version of the manuscript.
Figure 2 - Potential effects of exposure to radiofrequency
waves from a commercial smartphone on platelet
structure and biology.
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Blood Transfus DOI 10.2450/2016.0327-15
Acute effects of a smartphone on platelet function
Arrived: 12 December 2015 - Revision accepted: 21 December 2015
Correspondence: Giuseppe Lippi
Section of Clinical Biochemistry
University Hospital of Verona
Via delle Menegone, 10
37100 Verona, Italy
e-mail: giuseppe.lippi@univr.it
The Authors declare no conflicts of interest.
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... In hematology, the impact of EW of a mobile was also described in some parameters of complete blood count (CBC) after an exposure of 30 to 60 minutes of a sample. Some modifications were found particularly in polynuclear neutrophils structure and EW were considered as a potential source of preanalytical error [6][7][8][9][10][11]. ...
... This constatation can be induced by a fragmentation of other cells that can be counted as platelet. this modification has not been observed in human volunteers for which platelet rate remains unchanged as in the studies of Ahmed and Lippi after a chronic exposure to EW of a group of students [7,12]. However, an increase of platelet rate in rats after chronic exposure to EW was also described by many authors and explained it by a stimulation of megakaryopoiesis [13][14][15][16][17]. ...
... In blood sample, a raise of MPV was also found by Lippi who explained it by a probable platelet activation [7] while in our study, no change of MPV and other extended platelet parameters was found in in vivo and in vitro tests. Concerning leucocytes with differential count, no change was found excepting for neutrophil rate in in vitro test. ...
... The role of electromagnetic field theory in biology and medicine was an excellent introduction to electromagnetics in these sciences 6 . International Agency for Research on Cancer (IARC) and World Health Organization (WHO) conclude that the waves released from mobile phones are considered carcinogenic to humans, causing headaches, hearing loss and changes in brain activity 7,8 . Bioelectromagnetics fields interact with living systems which depends on the wave's shape, frequency and exposure time 9 . ...
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