Special Issue: Electromagnetic fields in biology and medicine

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A Correction to: Special Issue: Electromagnetic fields in biology and medicine

Background

This Special Issue presents the papers reporting further development of ideas delivered and discussed in the special session ‘Electromagnetic fields in biology and medicine’ during the joint conference of the 7th European Medical and Biological Engineering Conference (EMBEC7) and the 17th Nordic-Baltic Conference on Biomedical Engineering and Medical Physics (NBC17), held in Tampere, Finland, June 2017. The focus on the state-of-the-art presentations on non-thermal mechanism(s) and biological responses to electromagnetic field (EMF) exposure has been underlined in the call for papers of the EMF special session. Three sub-sessions provided an international forum for presenting and discussing the latest developments in EMF biological and health effects as well as EMF applications in medicine. The majority of authors are participating in the COST EMF-MED action ‘European network of innovative uses of EMFs in biomedical applications’.

In a modern society, the population is exposed to electromagnetic fields. A majority of people is exposed to radiofrequency (RF) radiation due to the widespread use of communication and information technologies: smart/mobile phones, Wi-Fi, internet of things etc. The employees and customers not only in industry but also during various public services can be exposed to intermediate (IR) or extra low-frequency (ELF) magnetic (MF) or electric fields (EF). People are accompanied with increasing numbers of monitoring and health supporting implanted or body-worn electronic devices and smart meters at home. The external EMF can, in principle, affect bioelectromagnetic processes that play a crucial role in biology and physiology at the molecular, cellular, and physiological systems level. Whether and how the external EMF affects biological and physiological processes and health has been a question of wide public interest during decades.

Numerous studies have been performed to investigate EMF effects and possible health risks of EMF exposure. Based on the results of scientific investigations, the International Agency for Research on Cancer has classified extremely low-frequency magnetic field as a possible human carcinogen in 2001 (IARC 2002) and radiofrequency EMF in 2011 (IARC 2013). Recently, the US National Toxicology Program Carcinogenesis Studies of Cell Phone Radiofrequency Radiation has published the results indicating increased cancer risk in rats (NTP 2018). Despite many years of studies and some success, there is still controversy over the low-level exposure effects, doubts in the possibility of non-thermal mechanism of radiofrequency EMF effect and uncertainties in the assessment of health risk. The problems are complicated due to complexity of living systems and large variation of exposure condition.

The thermal mechanism of radiofrequency EMF effects has been considered in the guidelines by the International Commission on Non-Ionizing Radiation Protection (ICNIRP; ICNIRP Guidelines 1998). The set by the ICNIRP reference levels has been followed by the authorities for health protection regulations in many countries. However, the findings reported in several studies in humans and animals (cellular stress, increase in free radicals, changes in DNA, functional changes in the reproductive system, alterations in the brain bioelectrical activity, learning and memory deficits etc.) at the levels of exposure below the thermal limits as well as several epidemiologic studies suggest the occurrence of EMF biological effects and the possibility of health effect at the levels of EMF exposure less than the set by the ICNIRP reference levels.

The scientific base for making decisions on possible health effects has still principal gaps. The concentration solely on thermal origin of the RF EMF effects in official regulations limits the interest of investigators toward the other possible mechanisms and the selection of new perspective research directions.

Addressing the raising concern of people related, first of all, to mobile telephony that has become commonplace around the world, the Parliamentary Assembly Council of Europe in its Resolution 1815 from 2011 recommends ‘reconsider the scientific basis for the present electromagnetic fields exposure standards set by the International Commission on Non-Ionising Radiation Protection, which have serious limitations and apply “as low as reasonably achievable” (ALARA) principles, covering both thermal effects and the athermic or biological effects of electromagnetic emissions or radiation’ (Parliamentary Assembly 2011). However, only few European countries and cities have followed the recommendation.

The main topics selected for the Special Issue cover some of important aspects of the area: physical and biological mechanisms of radiofrequency radiation effects by Hinrikus et al. and Herrala et al.; response to microwave radiation in physiological systems by Selmanoui et al. and Bachmann et al.; reproductive effects of intermediate frequency magnetic field by Khan et al.; low-frequency magnetic field effect on immune response by Wyszkowska et al. Special attention has been paid to medical applications of EMF including safety problems for implants in two papers by Zradzinski et al.; connectivity between surface and deep bioelectric fields in brain by Jäntti et al.; and practical use of EMF for toxicity assessment of biological suspensions by Muñoz et al.

The Editorial review of papers published in the Special Issue focuses on the interpretation of reported results and their adequacy according to the non-thermal mechanisms proposed by Hinrikus et al. for low-level RF EMF, based on the rotation of dipolar molecules, and published recently by Juutilainen et al. for low-level ELF MF, based on the rotation of radical pairs (Juutilainen et al. 2018). The proposed non-thermal mechanisms for the low-level EMF effects are expected to be fruitful for solving some principal controversies and explanation of uncertainties in experimental findings.

Threshold of low-level EMF effects

All experimental studies published in the Special Issue have been performed at the EMF levels lower than the reference levels for general public set by the ICNIRP. An only exception is the SAR value of 6 W/kg used as the higher level of exposure in the study by Herrala et al.

The ICNIRP Guidelines are based on thermal interaction mechanism for the RF EMF effects. Therefore, the rise of temperature inside tissue is the only criterion for the possibility of an EMF effect. The specific absorption rate (SAR) is a relevant parameter to describe the intensity of exposure in the case of thermal mechanism. The SAR value, corresponding to the fixed level of induced by EMF increase of temperature, can be considered as the threshold of the EMF effect induced by the thermal interaction mechanism.

In the case of non-thermal interaction mechanisms, the absorbed energy has no more direct linear relationship with the effect. Therefore, SAR becomes irrelevant as a parameter describing the threshold of the EMF effects. Parallel to SAR, the ICNIRP has set the reference levels for electric and magnetic fields strengths and EMF power spectral density, more relevant in the case of nom-thermal interaction mechanisms. Do the reference levels for EM field strengths set by ICNIRP determine the threshold of the non-thermal mechanism of EMF effects?

Rotations of dipolar molecules and radical pairs are known to be evident at the EMF strengths much less than the thermal threshold. The dielectric constant is assumed being constant, therefore, no threshold for dielectric polarization of a medium is expected at low-level exposure. The rotation of dipolar molecules can occur at very weak EMF. Radical pairs are known being sensitive to very weak magnetic fields, for example in birds. In the case of the rotation of dipolar molecules or radical pairs, the physical restrictions determining the minimal field strengths sufficient for the rotation are still unknown.

The threshold of the non-thermal mechanisms of EMF effects needs further theoretical and experimental investigations keeping in mind that the additional affecting factors can influence the threshold of low-level EMF. The oscillating nature of several biological structures, first of all, heart cells and neurons, makes possible parametric excitation of biological oscillations even by very weak periodic external EMF. The impact of parametric excitation depends not only on the strength of periodic force but rather more on the duration of excitation. Chaotic nature of biological systems creates a possibility that a very small initial change in a parameter of the system can cause remarkable alterations of the ongoing processes and finally results in a significant change in the status of the system. Due to diversity of living systems, the sensitivity to low-level EMF is expected to be different for individuals.

Combination of the EMF effects of thermal and non-thermal origin

In the case of EMF exposure, non-thermal and thermal mechanisms are working simultaneously. Even at low-level exposure, some thermal energy is generated but this is insufficient for increasing temperature inside a body. At high-level exposure, the rotation of dipolar molecules or radical pairs is evident but disturbed by thermal processes. Due to different nature of thermal and non-thermal effects and inertia of thermal processes, the non-thermal and thermal mechanisms can be related to different biological processes.

The results presented by Bachmann et al. demonstrate the direct impact of low-level modulated RF EMF in nervous system. The time constant of neuronal activity is about 1 ms, much longer than the period of RF EMF exposure. This is a reason, why neuronal processes can be affected only by modulated RF EMF and modulation is an important factor in many EMF studies. Bachmann et al. reported that the replicable modulated RF EMF stimuli induce response in the brain in the time scale characteristic for visual evoked potentials. Such a phenomenon cannot be caused by temperature due to inertia of thermal processes. On the other hand, the level of exposure is low enough for avoiding thermal effect disturbing the rotation of dipolar molecules.

The mobile phone radiation effect on skin conductance response to auditory stimuli, reported in the study by Selmaoui et al. is not so clearly caused only by non-thermal interaction mechanism. Despite low level of exposure, thermal energy in skin (the major part of RF EMF energy is absorbed in skin) increases during the exposure. The experiments were performed at SAR level about three times higher than in the study by Bachmann et al. Due to relatively large time constant of the skin conductance, lightly increased by the exposure skin temperature can cause a thermal effect. Thermal fluctuations disturb correlated with the EMF exposure rotation of molecules. As a result, the alterations in electrodermal activity are hardly detectable: the non-thermal interaction mechanism is suppressed by increased skin temperature, whereas thermal mechanism is not strong enough for being detectable.

Sometimes in experimental studies a ‘power window’ has been observed: caused by EMF alterations are increasing with exposure up to the certain level, but decreasing with the further increase of the exposure. The power window has been observable also in some results reported by NTP (NTP 2018).

The proposed by Hinrikus et al. non-thermal mechanism provides explanation of non-monotonic dependence of the EMF effect on the level of exposure. The window can be explained by combination of two different mechanisms of the effect, non-thermal and thermal. The rotational motion of dipolar molecules is a regular process driven by the electric field and, in principle, independent of random translational thermal motion and the thermal energy. However, the raising temperature increases collisions between molecules, and in this way disturbs dipolar polarization. The level of exposure, at which the disturbance becomes sufficient for decreasing polarization, determines the maximum of the power window.

Momentary or permanent effect

The study by Wyszkowska et al. indicated changes in blood and pro-inflammatory parameters in rats exposed to the ELF-MF 24 h per day during 7 days and no alterations in the parameters under the exposure of 1 h per day during 7 days. The reported results suggest long-lasting cumulative nature of the effect caused by exposure. In the case of only momentary effect, the results after exposure during one hour or 7 x 24 h are expected to be identical. The reported results suggest that the duration of exposure is important for the generation of detectable EMF effect.

No evidence of genomic instability from RF EMF exposure for 24 h has been reported by Herrala et al. The exposure at SAR levels 0.6 W/kg and 6.0 W/kg did not induce genomic instability in rat primary astrocytes. The exposure conditions in this paper were similar to these in the NTP studies except an important difference: the duration of exposure was much less than in the NTP study. The undetectable RF EMF effect would be explained by duration of exposure insufficient for generation genomic instability in rat primary astrocytes.

Both non-thermal mechanisms, proposed for ELF MF or RF EMF, are based on momentary phenomena, induced by EMF rotation of dipolar molecules or radical pairs. The rotations of dipolar molecules and radical pairs occur only during the exposure and stop when the exposure is switched off. The long-lasting alterations and permanent biological effects assume accumulation of small alterations, induced by EMF caused rotations in biological structures. The possible cumulative character of the EMF effects is supported by the mentioned above chaotic nature of processes in living systems and the possible parametric mechanism of excitation.

The hypothesis, that the duration of exposure is critical for generation of biological effects, suggests that the accumulation of small alterations, veiled in the case of short-term exposure, can result in remarkable biological effects during long-term exposure. The hypothesis needs further detailed investigations.

A large-scale epidemiological study on reproductive effects of IF MF exposure among cashiers working near electronic article surveillance systems, reported by Khan et al., did not discover the risk of miscarriage, reduced birth weight or preterm birth. According to the hypotheses of long exposure duration, discussed above, the effects of IF MF are expected to be evident in the case of long-term occupational exposure. In the case of the reported study, only differences in the limited number of indicators, not related to the physiological parameters of women, have been assessed. Therefore, the published data do not confirm the missing effect on the health of women. On the other hand, the reported by Khan et al. conclusions are in accordance with the NTP results where no tumors have been detected in female rats.

The time interval from the revealed biological effects to health effects might be much longer than the accumulation time, required for detection of the effect. For example, the time interval can be about ten years in the case of cancerous processes. The determining of the initial origin of the health disorder becomes difficult or even impossible.

EMF in passive medium and living tissues

The modeling and calculation of EMF parameters based on a passive human or animal model with predefined dielectric and conductivity parameters’ values for different tissue types. The dielectric parameters are known to be different for living and post-mortem tissues. Muñoz et al. demonstrated, that even small variation of the complex permittivity of the biological suspensions makes possible to identify viable and non-viable embryos after a toxic exposure.

The results of modeling of ELF and IF MF exposure near the insulin pump needle, reported by Zradziński et al., demonstrate that even the small implanted devices significantly change the structure of EMF inside the body. Much more strict regulations for EMF radiation level are required in the case of implants. The inter-person differences in body structure and parameters induce remarkable variability in the exposure to ELF MF (Zradziński). Therefore, individual assessment of the EMF health risk can be recommended in the case of implanted and wearable medical devices.

In the case of RF EMF, the depth of penetration of the field into a passive medium of high dielectric properties is limited to skin-effect. The field strength becomes small in deeper body structures and the EMF effect is expected being limited to surface layers. However, in living tissue, the processes activated by EMF in the surface layers can be connected with and affect the processes in much deeper systems.

The study performed by Jäntti et al. in anesthesia electroencephalography demonstrate, that the bioelectric signals created by anesthetic drug in deep brain structure can be detected not only by deep electrodes but also by electrodes in brain surface. This finding demonstrates the connectivity of bioelectric processes in various spatial locations: the fields in deep brain structures causes response in its surface. According to the principle of reciprocity, the surface fields are expected to cause response in the fields in deep structures. There is a high possibility that the EMF effects in tissues are not limited to the depth of skin-layer.

The ongoing discussions about 5G technology are based on a presumption that, due to very thin skin-layer, the EMF effect occurs only in human skin. However, in the case of real living systems, the processes in different tissues are interconnected. Therefore, excited by EMF skin structures are physiologically connected to deeper systems in body and the affected space can be much deeper.

Recommendations for further research

The analysis of even very limited number of papers has been useful for identifying some important gaps in the existing knowledge about EMF effects. Some recommendations for further investigations can be outlined.

1. Different nature of the non-thermal and thermal mechanisms of EMF effects requires the reconsideration of the measures and indicators for the assessment of health risk. The complex approach, based on the non-thermal mechanism and the specific nature of living system, is expected to be fruitful. New ideas for non-thermal measures and possible biological indicators are highly requested.

2. The effects of low-level RF EMF on hydrogen bonding and related possible consequences in DNA instability and neurodegenerative processes, including the impact of cumulative and parametric effects, require most attention. The theoretical, as well as experimental studies would be useful.

3. More detailed investigation of combined non-thermal and thermal mechanisms of RF EMF effects, so-called ‘window’ effect, would be fruitful for understanding the processes and their possible biological consequences.

4. The interconnectivity of EMF caused alterations in skin-layer and deep structures require investigation, especially in the case of non-thermal mechanisms of the effect induced by low-level exposure.

5. The problems related to long-term exposure and health risks from chronic exposures are still actual.

Acknowledgments

The Guest Editors appreciate the efforts, support, and patience of all authors, reviewers and managing editors, who contributed to this Special Issue.

Disclosure statement

No potential conflict of interest was reported by the authors.