Introduction

Life evolved in a radiation environment that was either harmless or caused adaptation. Over the past 3.5 billion years, the forms of life evolved starting from the first cells to the emergence of mankind in an environment filled with different ionizing and non-ionizing radiations [ 1 - 3 ]. While the ambient dose rates at the early days of life (~10 times higher than today) accounted for up to 33% of mutations of the first forms of life, current background radiation accounts only for 1–6% of the mutations [ 4 , 5 ]. Due to higher concentrations of radionuclides, and the existence of “natural reactors” (e.g. those remaining found in the Oklo and Bangombédeposits of the Franceville basin in Gabon, Western Africa), the levels of ionizing radiation were generally higher on Earth in the early days of life than nowadays [ 6 ].

Adaptive Response (AR) can be defined as an increased resistance to high levels of a stressor (physical or chemical) after exposure to a low-level stress (either the same stressor or other types of stress) [ 7 , 8 ]. The applications of this phenomenon in different fields, including, but not limited to, the treatment of tumors, risk management, and in particular radiation protection are well-documented. Studies performed on the AR triggered by small doses of ionizing radiation show the initiation of several signaling pathways, change in gene transcription, specific protein synthesis, increased antioxidant production, free radical release and detoxification. As a consequence, these potential cellular mechanisms induce DNA repair systems and cell defenses that can be considered underlying the phenomenon of AR (Figure 1). In this mini-review, we address certain unresolved questions concerning adaptive response in bacteria focusing on the radiofrequency-induced adaptive response.

Figure 1. Schematic illustration of adaptive response. Pre-exposure of cells to a low-level stressor (e.g., low-dose ionizing radiation such as X-rays, and/or gamma rays, or non-ionizing radiations such as radiofrequency radiation) increases their resistance against a following high-level stressor (e.g., high dose radiation).

Effects of electromagnetic fields on bacteria

Electromagnetic Fields (EMF) can cause biological effects on exposed microorganisms, which can potentially induce either an inhibiting or a stimulating response. There are two main categories of biological effects: thermal and non-thermal effects. The manifestation of one type of these effects on microorganisms depends on the power and frequency of the electromagnetic field [ 9 ]. Ionizing radiations (such as gamma rays, X-rays, and particle radiation) are generally accompanied by thermal effects, which have energies high enough to ionize certain molecules. As a consequence, the temperature rises by more than 1 °C, causing intracellular changes, which might induce heat-stress-related responses [ 10 ]. For non-ionizing radiation, the effects do not cause an increase in temperature due to the lower frequency and are therefore non-thermal effects. Among non-ionizing radiation, the most common public sources are extremely low-frequency electromagnetic fields that are commonly used in the transmission of electric power and Radiofrequency (RF), which compromise mobile communication systems and Wi-Fi waves [ 11 ]. The mechanisms of RF-induced non-thermal effects on bacteria are not well-known and seem to have multiple origins. Some hypotheses evoke cellular and physiological changes at many levels: growth rate, metabolism, cell membrane integrity, antibiotic sensitivity, biofilm formation, gene expression, and others. Table 1 summarises the non-thermal effects of radiofrequency radiation (mobile phones, Wi-Fi routers, and mobile base stations) on various bacterial species.

1. Effects of RF on bacterial growth

EMF, and other environmental stressors, have been reported to affect the growth of bacteria (Table 1). The effects of EMF on bacterial growth depend on numerous parameters: the frequency, wavelength, intensity, pre- or post-exposure, and duration of exposure [ 26 ]. Some studies on RF-EMF have shown an increase in the viability of various bacterial strains by triggering their growth rate [ 20 , 25 ]. However, other reports showed that these radiations decrease bacterial cell growth [ 13 , 17 , 27 ]. The contradicting results have caught the interest of several researchers who have concentrated on the aseptic action of higher-frequency waves [ 28 , 29 ]. The bactericidal effects of electromagnetic waves on oral bacterial pathogens have been investigated, and according to Yumoto et al. irradiation at 500 kHz may be used for disinfection and sterilization purposes [ 30 ].

2. Effect of RF on bacterial susceptibility to antibiotics

The prospective use of specific antibiotics with induced synergistic and/or antagonistic effects in response to EMF has gotten special attention given the threat that antibiotic resistance represents to public health. This has also been addressed by the World Health Organization (WHO) [ 31 ]. Global System for Mobile Communications (GSM) and Wi-Fi radiations appear to induce resistance to antibiotics in some bacteria [ 14 , 15 , 18 , 22 ]. Moreover, continuous 24-hour’s exposure to GSM mobile waves induced P. aeruginosa to become persisters bacteria (a subpopulation of transiently antibiotic-tolerant bacterial cells that are often slow-growing or growth-arrested, and are able to resume growth after a lethal stress [ 32 ]) with enhanced antibiotic resistance. Exposed bacteria were able to resume growth with transient antibiotic tolerance after radiofrequency radiation stress [ 15 ]. Conversely, 2 hours GSM exposure revealed no important change in the antibiotic susceptibility of exposed S. epidermidis [ 17 ]. Furthermore, Wi-Fi radiation has shown a significantly higher susceptibility of Klebsiella pneumoniae to several antibiotics (Aztreonam, Cefteriaxone, Imipenem, Piperacillin, and Cefotaxime) before they reached an adaptation stage (a stage in which bacteria became forced to adapt to its environment) [ 14 ]. Some studies have reported that altered antibiotic resistance is related to substantial changes in the bacterial membrane and cell wall composition due to radiation exposure [ 14 , 22 , 33 ]. RF radiation may influence the mechanisms of antibiotic efflux by pumping out the antibiotic to the external environment using transporter proteins and activating Save-Our-Soul (SOS) response in bacteria (Figure 2) [ 19 , 34 ]. The upregulation of the genes ybhG, ampE, and some ABC transporters was reported in E. coli after 5 hours of Wi-Fi exposure [ 19 ] where ybhG is implicated in the control of susceptibility to chloramphenicol through the efflux pathway [ 35 ] and ampE is involved in peptidoglycan murein recycling by the expression of β-lactamase [ 36 , 37 ]. Therapeutically, scientists validated that the effect of several antibiotics on bacteria could be enhanced synergically using Higher frequency of EMF from the ranges of 70-75 GHz [ 26 , 38 ].

Figure 2. Potential effect of radiofrequency on bacterial antibiotic resistance. Radiofrequency (RF) Radiation damages the cell membrane and increases reactive oxygen species (ROS) in the cell. Alternatively, radiofrequency radiation activates Save-Our-Soul (SOS) response and antibiotic efflux pumps as mechanisms of defense and repair in bacteria.

3. Effect of RF on bacterial DNA

DNA impairment and genotoxicity induced by EMFs have been intensively studied in organism models, such as for microorganisms, animals and plants [ 39 ]. The results revealed some possible mutagenic effects of low-frequency EMFs on Salmonella typhimurium [ 40 ]. Results obtained in this study showed a higher number of revertants in the presence of the magnetic field up to 18-fold compared to control plates. Furthermore, exposure of E. coli to magnetic fields can activate DNA repair by the induction of chaperone protein DnaK synthesis in response to the applied stress by 20 % repair improvement [ 41 ], while exposure of bacteria to RF at 0.835 GHz revealed no change in the reversion frequency neither in the DNA degradation in vitro using Ames method [ 12 ]. In parallel, 5 hours of Wi-Fi radiofrequency exposure upregulated sulA, yjjQ, oxC and arsC genes which are part of the defense system against DNA damage (SOS response) and 11 transposition-related genes as a response to the environmental radiation [ 19 ] (Figure 2).

4. Effect of RF on bacterial cell morphology

Microscopic analyses have revealed that bacterial cells exposed to EMF exhibited different cell morphology than unexposed controls. For example, E. coli cells exposed to microwave radiation at 18 GHz and at a temperature below 40 °C appeared dehydrated and shrunken compared to those not exposed, and even similar to those thermally heated (40 °C) [ 42 ]. The effect of these radiations was temporary and returned to the original state after 10 min. Similar effects were observed in Wi-Fi-exposed K. pneumoniae such as disruption of the protoplasm and plasma membrane [ 22 ]. The use of electrical and RF fields has been also applied in therapeutical treatments such as heart arrhythmias and tumor therapies [ 43 ].

5. Effects of RF on bacterial motility and chemotaxis

Motility is one of the strategies used by bacteria to escape environmental stressors. These prokaryotic cells can move by using their pili for gliding and twitching or their flagella for swimming [ 44 ]. Bacterial flagella are well-studied at the structural and molecular levels. Their movement has been shown to be powered by a rotational motor at their organizing centers, where 20 and 30 proteins are required to assemble and control the flagellar rotation [ 45 ]. Upon exposure to an environmental stimulus, bacteria can perceive the changes in their environment and therefore, they respond by deviating their motility that becomes directed toward a more favourable environment through a process known as chemotaxis [ 46 ].

In a recent study, the effect of RF on the motility of E. coli 0157H7 has been assessed by soft agar assay. As compared to non-exposed E. coli, the data demonstrates that motility has been dramatically enhanced by 28% and 29% over 24 and 48 hours of Wi-Fi exposure, respectively [ 18 ]. The outcomes of this study are consistent with previous research that demonstrated a substantial increase in E. coli motility under acid and heat stress [ 47 , 48 ]. Furthermore, next-generation sequencing data revealed that exposure to Wi-Fi waves increased the expression of genes involved in chemotaxis and motility, including fiA, fgM, motB, fiC, cheY, cheR, fiM, fiL, fgG, and fiT with the higher Enrichment Score (ES) in DAVID functional clustering [ 19 ].

6. Effects of RF on bacterial biofilm formation

Another aspect of physiological changes that the microorganisms undergo in response to different environmental stress factors is the biofilm formation. In this process, cells expressing a biofilm phenotype exhibit resistance to environmental stress conditions [ 49 ].

Biofilm formation occurs through at least three different mechanisms: (1) the attachment to the surface, (2) the multiplication and maturation of attached cells, and (3) the detachment and recruiting of cells from the bulk fluid [ 50 ]. In a biofilm environment, bacteria appear to be over a thousand times more resistant to a particular antibiotic than the same planktonic strains. It has been shown that RF at 10 MHz can increase the efficacy of antibiotics in E. coli biofilms [ 51 ]. However, short time exposure of S. aureus to GSM did not influence their biofilm production [ 13 ]. Rotating magnetic field increased biofilm formation by S. aureus and E. coli [ 52 ]. Similar results were revealed with exposure to RF showing an alteration in biofilm formation [ 14 , 16 , 18 ]. In addition, exposure to Wi-Fi waves significantly increased the expression of the representative genes (luxS, mrkA, and bcsA) involved in biofilm formation and quorum sensing by 1 to 1.8 fold in K. pneumoniae [ 22 ].

7. Effects of RF on bacterial heat shock response

Heat Shock Proteins (HSPs) are present and conserved in all living organisms, from bacteria to humans [ 53 ]. They control and regulate cellular processes to protect the cell from environmental stress. Research laboratories have conceived numerous experimental models (in-vivo and in-vitro) to find possible biomarkers that are sensitive to physical stimuli and potential risks of EMF exposure. Henschenmacher et al. assessed the relationship between exposure to RF and oxidative stress through a meta-analysis study [ 54 ]. HSPs are known as “stress proteins” and are used as environmental biomarkers [ 55 ]. The level of expression of Dnak (equivalent to human HSP70) in E. coli was significantly raised after exposure to RF exposure. The study conducted by Aoude et al. using RF non-thermal effect revealed that Dnak and lacZ gene expression in exposed samples were higher at the level of mRNA using Reverse Transcription Polymerase Chain Reaction (RT-PCR) [ 56 ].

8. Effects of RF on bacterial gene expression

There are only a few studies of EMF effects on gene and protein expression in bacteria. Exposure to low-frequency EMF modifies slightly the global protein expression of Chromobacterium violaceum [ 57 ]. The results of the study conducted by El May in 2009, using a Static Magnetic Field (SMF) on cell growth, viability, and differential gene expression in Salmonella showed that the involved proteins were associated with protection against DNA damage and cellular metabolism. Moreover, exposure of Salmonella hadar to SMF showed a stress response mediated by an up-regulation of the rpoA, katN, and dnaK genes [ 58 ]. Next-generation RNA sequencing experiment conducted by Said-Salman et al. revealed that the exposure of E. coli DH5α to RF waves influenced 101 genes that are implicated in different metabolic and cellular mechanisms, stress adaptation, transposition, response to stimuli, and matrix adhesion [ 19 ]. In this research, 52 upregulated genes were mainly involved in stress adaptation such as motility and chemotaxis while the downregulated genes were essentially related to metabolic processes [ 19 ].

Bacterial Radio-adaptation

1. Adaptation of bacteria to ionizing radiation

To investigate the susceptibility of microorganisms to antibiotics after exposure to gamma radiation, Mortazavi et al. exposed different bacterial samples of S. typhimurium, S. aureus, and K. pneumoniae to gamma rays emitted from soil collected from the high background radiation areas of Ramsar in Northern Iran [ 59 ]. While the mean diameter of no growth zone, in the standard Kirby-Bauer test, was 20.3±0.6 mm in non-irradiated K. pneumoniae control samples; it was only 14.7±0.6 mm in irradiated bacteria. The authors concluded that exposure to gamma rays significantly changed bacterial susceptibility to antibiotics. They hypothesized that natural background radiation was able to induce adaptive phenomena that helped bacteria better cope with the inhibitory effects of antibiotics.

2. Adaptation of bacteria to non-ionizing radiofrequency radiation

As shown in Figure 3, besides mechanical waves, such as diagnostic ultrasound [ 60 ], and pre-exposure to low-level ionizing electromagnetic radiation (e.g., gamma rays) [ 59 ], evidence shows that bacteria develop different mechanisms of adaptation to non-ionizing electromagnetic Radiofrequency (RF) such: antibiotic resistance, biofilm formation, altered growth, differentiated gene expression, and cell membrane impairment (Table 1). Bacteria that have become radioadapted not only developed more resistance to higher doses of radiation (such as mobile phone and Wi-Fi) but also resistance to any other factor that can be fatal for bacteria (e.g. antibiotics) [ 14 , 18 , 22 , 61 ]. There are more than 8 billion mobile subscriptions in use worldwide in 2022 [ 62 ]. Bacteria have developed over the years around 800 proteins that contribute to antibiotic resistance as stated by the Centers for Disease Control and Prevention (CDC) Antimicrobial Threats Report [ 63 ], which correlate with the increased number of RF-EMF (mobile phone, Wi-Fi, base stations,…) (Figure 4).

Figure 3. In addition to mechanical waves like diagnostic ultrasound, and exposure to ionizing radiations (e.g., gamma rays), research indicates that bacteria exhibit various adaptation mechanisms to non-ionizing electromagnetic radiation (e.g., radiofrequency) observed as antibiotic resistance, biofilm formation, changes in growth patterns, modified gene expression, and impairment of cell membranes.

Figure 4. Cumulative number of beta-lactamase enzymes identified in bacteria in correlation with the estimated number of mobile phone subscriptions over the past years.

EMF Biohazard

Due to the difficulties of reproducing the exact parameters of published experiments, the effects of EMF on biological systems (bacteria, plants, or cellular cultures…) have generated several disagreements. There is a substantial debate about whether the EMFs are detrimental or advantageous to human health; several in vivo and in vitro studies revealed that non-ionizing radiation might have a negative impact on human health [ 64 ]; however, others suggested a beneficial effect of EMF [ 65 ]. The WHO has advised the assessment of the biological effects of the prevailing EMF radiation in inhabitants before authorizing the settlement of new EMF networks [ 66 ]. Another concern is that the exposure limits that have been set by regulatory agencies based on experiments using radiation in isolated spaces not taking into consideration other environmental toxic stimuli (biological and chemical). The set exposure limits would be in this case much lower for risk-free use. In a toxicology letter, Kostoff et al. reported that under real-life conditions, other toxic stimuli should be considered in combination with the new 5G wireless networking technology, which will increase the hazardous effects related to only RF exposure [ 67 ].

Mechanisms of bacterial adaptation to electromagnetic radiation

Based on screened data revealed in previously published studies conducted with the aim to evaluate the effects of radiofrequency radiation on microorganisms (Table 1), we hereby propose a potential mechanism for bacterial adaptation to surrounding radiation. Pre-exposure of bacteria to a low-level radiation might increase their resistance against a high-level radiation by activating a bacterial regulatory network in response to EMF, as shown in Figure 5-a. Under environmental radiation stress, a microorganism may alternate between the stages of proliferation and slow proliferation to resist the applied environment. Some of the bacterial communities go into a dormant state (Figure 5-b). At this stage, bacteria preserve a part of their metabolic activity but they become unable to replicate as a consequence of their slight adjustment ability. Modifications in the bacterial gene expression enable bacteria to counter the stress circumstances by shutting down their metabolism and arresting their growth in order to survive [ 19 ]. Other persistence mechanisms could be generated in response to environmental stress such as SOS repair, efflux pump and ability to form biofilm [ 68 - 71 ].

Figure 5. Suggested mechanisms of bacterial resistance to electromagnetic radiation. (a) Schematic representation of bacterial adaption to high level radiation after pre-exposure to low-level radiation (b) Schematic representation of bacterial regulatory network activated in response to radiation.

Discussion

It has been shown that the range of antimicrobial concentrations known as “the mutant selection window” extends from the lowest concentration needed to prevent the growth of wild-type bacteria to the highest concentration needed to prevent the growth of the least susceptible mutant [ 72 ]. Limiting the enrichment of mutants is achieved by maintaining antimicrobial concentrations above the window [ 73 ]. The idea was also adapted for radiation biology. The exposure to radiofrequency should be within a narrow level of exposure and exposure rate (the so-called “exposure window theory”) to turn microorganisms resistant to antibiotics. This type of multi-phasic response is similar to the responses induced by ionizing radiation. Mortazavi has previously shown that the findings of some experiments on pre-exposure to radiofrequency radiation support the existence of a minimum level of damage to trigger an adaptive response [ 74 ]. According to the exposure window theory, the induction of adaptive responses only occurs when the exposure(s) rates are within a specific window [ 14 ]. Given this consideration, Mortazavi has reported that these responses are similar to those frequently reported for induction of adaptive response by ionizing radiation [ 59 ]. Regarding adaptive responses induced by ionizing radiations, Mitchel has previously reported that “the adaptive response in mammalian cells and mammals operates within a certain 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” [ 75 ].

Conclusion

The exposure of bacteria to EMF can be appreciated when altering with bacterial survival mechanism and may compromise therapeutic success. However, continuous exposure of microorganisms to common sources of EMF such RF may emerge super-pathogens with high resistance to treatments.

Authors’ Contribution

I. Said-Salman provided the conceptualization, original draft preparation, review and editing. SMJ worked on the original draft preparation, review, and editing. SAR. Mortazavi did review and editing. S. El Khatib did review, and editing. L. Sihver wrote the draft, reviewed the manuscript, edited and submitted the final version of the paper. All authors reviewed the final version of the manuscript.

Funding

None

Conflict of Interest

SMJ. Mortazavi and L. Sihver, as the Editorial Board Members, were not involved in the peer-review and decision-making processes for this manuscript.

References

1. Mortazavi SMJ, Ghiassi-nejad M, Niroomand-rad A, Karam PA, Cameron JR. How Should Governments Address High Levels of Natural Radiation and Radon--Lessons from the Chernobyl Nuclear Accident and Ramsar, Iran. Risk. 2002; 13:31.
2. Steinhauser G. Ionizing radiation—an evolutionary threat. Hypothesis. 2015; 13(1):e6.
3. Dobrzyński L, Fornalski KW, Feinendegen LE. Cancer Mortality Among People Living in Areas With Various Levels of Natural Background Radiation. Dose Response. 2015; 13(3):1559325815592391. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
4. Karam PA, Leslie SA. Calculations of background beta-gamma radiation dose through geologic time. Health Phys. 1999; 77(6):662-7. DOI | PubMed
5. Abbasi S, Mortazavi SAR, Mortazavi SMJ. Martian Residents: Mass Media and Ramsar High Background Radiation Areas. J Biomed Phys Eng. 2019; 9(4):483-6. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
6. Gauthier-Lafaye F, Holliger P, Blanc PL. Natural fission reactors in the Franceville basin, Gabon: A review of the conditions and results of a “critical event” in a geologic system. Geochim Cosmochim Acta. 1996; 60(23):4831-52. DOI
7. Mortazavi SMJ, Motamedifar M, Namdari G, Taheri M, Mortazavi SAR, Shokrpour N. Non-linear adaptive phenomena which decrease the risk of infection after pre-exposure to radiofrequency radiation. Dose Response. 2013; 12(2):233-45. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
8. Dimova EG, Bryant PE, Chankova SG. Adaptive response: some underlying mechanisms and open questions. Genet Mol Biol. 2008; 31:396-408. DOI
9. Salmen SH. Non-Thermal Biological Effects of Electromagnetic Field on Bacteria-A. Am J Res Commun. 2016; 4:16-28.
10. Vecchia P, Matthes R, Gunde Ziegelberger, Lin J, Saunders R, Swerdlow A. Exposure to high frequency electromagnetic fields, biological effects and health consequences (100 kHz-300 GHz). Germany: International Commission on Non-Ionizing Radiation Protection; 2009.
11. Omer H. Radiobiological effects and medical applications of non-ionizing radiation. Saudi J Biol Sci. 2021; 28(10):5585-92. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
12. Chang SK, Choi JS, Gil HW, Yang JO, Lee EY, Jeon YS, et al. Genotoxicity evaluation of electromagnetic fields generated by 835-MHz mobile phone frequency band. Eur J Cancer Prev. 2005; 14(2):175-9. DOI | PubMed
13. Mohd-Zain Z, Mohd-Ismail MS, Buniyamin N. Effects of mobile phone generated high frequency electromagnetic field on the viability and biofilm formation of Staphylococcus aureus. International Scholarly and Scientific Research & Innovation. 2012; 6(10):871-4.
14. Taheri M, Mortazavi SMJ, Moradi M, Mansouri Sh, Nouri F, Mortazavi SAR, Bahmanzadegan F. Klebsiella pneumonia, a Microorganism that Approves the Non-linear Responses to Antibiotics and Window Theory after Exposure to Wi-Fi 2.4 GHz Electromagnetic Radiofrequency Radiation. J Biomed Phys Eng. 2015; 5(3):115-20. Publisher Full Text | PubMed [ PMC Free Article ]
15. Nakouti I, Hobbs G, Teethaisong Y, Phipps D. A demonstration of athermal effects of continuous microwave irradiation on the growth and antibiotic sensitivity of Pseudomonas aeruginosa PAO1. Biotechnol Prog. 2017; 33(1):37-44. DOI | PubMed
16. Taheri M, Mortazavi SMJ, Moradi M, Mansouri S, Hatam GR, Nouri F. Evaluation of the Effect of Radiofrequency Radiation Emitted From Wi-Fi Router and Mobile Phone Simulator on the Antibacterial Susceptibility of Pathogenic Bacteria Listeria monocytogenes and Escherichia coli. Dose Response. 2017; 15(1):1-8. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
17. Salmen SH, Alharbi SA, Faden AA, Wainwright M. Evaluation of effect of high frequency electromagnetic field on growth and antibiotic sensitivity of bacteria. Saudi J Biol Sci. 2018; 25(1):105-10. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
18. Said-Salman IH, Jebaii FA, Yusef HH, Moustafa ME. Evaluation of Wi-Fi Radiation Effects on Antibiotic Susceptibility, Metabolic Activity and Biofilm Formation by Escherichia Coli 0157H7, Staphylococcus Aureus and Staphylococcus Epidermis. J Biomed Phys Eng. 2019; 9(5):579-86. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
19. Said-Salman IH, Jebaii FA, Yusef HH, Moustafa ME. Global gene expression analysis of Escherichia coli K-12 DH5α after exposure to 2.4 GHz wireless fidelity radiation. Sci Rep. 2019; 9(1):14425. DOI
20. Amanat S, Mazloomi SM, Asadimehr H, Sadeghi F, Shekouhi F, Mortazavi SMJ. Lactobacillus Acidophilus and Lactobacillus Casei Exposed to Wi-Fi Radiofrequency Electromagnetic Radiation Show Enhanced Growth and Lactic Acid Production. J Biomed Phys Eng. 2020; 10(6):745-50. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
21. Cordero-Samortin A, Cruz JC, Garcia R, Mabunga Z. The effect of various ultra high frequency radiation on the evolution of the staphylococcus aureus. In 12th International Conference on Humanoid, Nanotechnology, Information Technology, Communication and Control, Environment, and Management (HNICEM); Manila, Philippines: IEEE; 2020.
22. Said-Salman I, Yassine W, Rammal A, Hneino M, Yusef H, Moustafa M. Effects of Wi-Fi Radiofrequency Radiation on Carbapenem-Resistant Klebsiella pneumoniae. Bioelectromagnetics. 2021; 42(7):575-82. DOI | PubMed
23. Pegios A, Kavvadas D, Ζarras K, Mpani K, Soukiouroglou P, Charalampidou S, et al. The Effect of Electromagnetic Radiation Transmitted from Routers on Antibiotic Susceptibility of Bacterial Pathogens. J Biomed Phys Eng. 2022; 12(4):327-38. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
24. Bujňáková D, Bucko S, Češkovič M, Kmeť V, Karahutová L. The effect of exposure to non-ionising radiofrequency field on Escherichia coli, Klebsiella oxytoca and Pseudomonas aeruginosa biofilms. Environ Technol. 2023; 44(25):3813-9. DOI | PubMed
25. Mortazavi SMJ, Taheri M, Paknahad M, Khandadash S. Effects of Radiofrequency Electromagnetic Fields Emitted from Mobile Phones and Wi-Fi Router on the Growth Rate and Susceptibility of Enterococcus faecalis to Antibiotics. J Biomed Phys Eng. 2022; 12(4):387-94. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
26. Torgomyan H, Trchounian A. Low-intensity electromagnetic irradiation of 70.6 and 73 GHz frequencies enhances the effects of disulfide bonds reducer on Escherichia coli growth and affects the bacterial surface oxidation-reduction state. Biochem Biophys Res Commun. 2011; 414(1):265-9. DOI | PubMed
27. Cranfield C, Wieser HG, Al Madan J, Dobson J. Preliminary evaluation of nanoscale biogenic magnetite-based ferromagnetic transduction mechanisms for mobile phone bioeffects. IEEE Trans Nanobioscience. 2003; 2(1):40-3. DOI | PubMed
28. Woo IS, Rhee IK, Park HD. Differential damage in bacterial cells by microwave radiation on the basis of cell wall structure. Appl Environ Microbiol. 2000; 66(5):2243-7. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
29. Apostolou I, Papadopoulou C, Levidiotou S, Ioannides K. The effect of short-time microwave exposures on Escherichia coli O157:H7 inoculated onto chicken meat portions and whole chickens. Int J Food Microbiol. 2005; 101(1):105-10. DOI | PubMed
30. Yumoto H, Tominaga T, Hirao K, Kimura T, Takahashi K, Sumitomo T, et al. Bactericidal activity and oral pathogen inactivation by electromagnetic wave irradiation. J Appl Microbiol. 2012; 113(1):181-91. DOI | PubMed
31. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS). World Health Organization; 2022.
32. Fisher RA, Gollan B, Helaine S. Persistent bacterial infections and persister cells. Nat Rev Microbiol. 2017; 15(8):453-64. DOI | PubMed
33. Ayari S, Dussault D, Millette M, Hamdi M, Lacroix M. Changes in membrane fatty acids and murein composition of Bacillus cereus and Salmonella Typhi induced by gamma irradiation treatment. Int J Food Microbiol. 2009; 135(1):1-6. DOI | PubMed
34. Amani S, Taheri M, Movahedi MM, Mohebi M, Nouri F, Mehdizadeh A. Evaluation of Short-Term Exposure to 2.4 GHz Radiofrequency Radiation Emitted from Wi-Fi Routers on the Antimicrobial Susceptibility of Pseudomonas aeruginosa and Staphylococcus aureus. Galen Med J. 2020; 9:e1580. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
35. Yamanaka Y, Shimada T, Yamamoto K, Ishihama A. Transcription factor CecR (YbiH) regulates a set of genes affecting the sensitivity of Escherichia coli against cefoperazone and chloramphenicol. Microbiology (Reading). 2016; 162(7):1253-64. DOI | PubMed
36. Lindquist S, Galleni M, Lindberg F, Normark S. Signalling proteins in enterobacterial AmpC beta-lactamase regulation. Mol Microbiol. 1989; 3(8):1091-102. DOI | PubMed
37. Park JT, Uehara T. How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev. 2008; 72(2):211-27. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
38. Torgomyan H, Trchounian A. Bactericidal effects of low-intensity extremely high frequency electromagnetic field: an overview with phenomenon, mechanisms, targets and consequences. Crit Rev Microbiol. 2013; 39(1):102-11. DOI | PubMed
39. McCann J. Cancer risk assessment of extremely low frequency electric and magnetic fields: a critical review of methodology. Environ Health Perspect. 1998; 106(11):701-17. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
40. Tabrah FL, Mower HF, Batkin S, Greenwood PB. Enhanced mutagenic effect of a 60 Hz time-varying magnetic field on numbers of azide-induced TA100 revertant colonies. Bioelectromagnetics. 1994; 15(1):85-93. DOI | PubMed
41. Chow K, Tung WL. Magnetic field exposure enhances DNA repair through the induction of DnaK/J synthesis. FEBS Lett. 2000; 478(1-2):133-6. DOI | PubMed
42. Shamis Y, Taube A, Mitik-Dineva N, Croft R, Crawford RJ, Ivanova EP. Specific electromagnetic effects of microwave radiation on Escherichia coli. Appl Environ Microbiol. 2011; 77(9):3017-22. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
43. Schoenbach KH. From the basic science of biological effects of ultrashort electrical pulses to medical therapies. Bioelectromagnetics. 2018; 39(4):257-76. DOI | PubMed
44. Bardy SL, Ng SYM, Jarrell KF. Prokaryotic motility structures. Microbiology (Reading). 2003; 149(Pt 2):295-304. DOI | PubMed
45. Aldridge P, Hughes KT. Regulation of flagellar assembly. Curr Opin Microbiol. 2002; 5(2):160-5. DOI | PubMed
46. Hansen CH, Endres RG, Wingreen NS. Chemotaxis in Escherichia coli: a molecular model for robust precise adaptation. PLoS Comput Biol. 2008; 4(1):14-27. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
47. Chung HJ, Bang W, Drake MA. Stress response of Escherichia coli. Compr Rev Food Sci Food Saf. 2006; 5(3):52-64.
48. House B, Kus JV, Prayitno N, Mair R, Que L, Chingcuanco F, et al. Acid-stress-induced changes in enterohaemorrhagic Escherichia coli O157: H7 virulence. Microbiology (Reading). 2009; 155(Pt 9):2907-18. DOI | PubMed
49. Mah TF, O’Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 2001; 9(1):34-9. DOI | PubMed
50. Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu Rev Microbiol. 2002; 56:187-209. DOI | PubMed
51. Caubet R, Pedarros-Caubet F, Chu M, Freye E, De Belém Rodrigues M, Moreau JM, Ellison WJ. A radio frequency electric current enhances antibiotic efficacy against bacterial biofilms. Antimicrob Agents Chemother. 2004; 48(12):4662-4. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
52. Fijalkowski K, Nawrotek P, Struk M, Kordas M, Rakoczy R. The effects of rotating magnetic field on growth rate, cell metabolic activity and biofilm formation by Staphylococcus aureus and Escherichia coli. Journal of Magnetics. 2013; 18(3):289-96. DOI
53. Morimoto RI, Westerheide SD. The heat shock response and the stress of misfolded proteins. In Handbook of cell signalling. Elsevier; 2010. p. 269-75.
54. Henschenmacher B, Bitsch A, De Las Heras Gala T, Forman HJ, Fragoulis A, Ghezzi P, et al. The effect of radiofrequency electromagnetic fields (RF-EMF) on biomarkers of oxidative stress in vivo and in vitro: A protocol for a systematic review. Environ Int. 2022; 158:106932. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
55. Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH. Stress proteins (HSP’s): methods of detection and their use as an environmental biomarker. Ecotoxicology. 1999; 8(5):351-68. DOI
56. Aoude I, Saab S, Aoude N, Mortada M, Jebai F, Ezzeddine M. RF-MW non-thermal effect enhanced Beta-galactosidase expression through the induction of Dnak synthesis in E. coli BL21 DE3. Wseas Transactions On Biology And Biomedicine. 2008; 5(9): 221-8.
57. Baraúna RA, Santos AV, Graças DA, Santos DM, Ghilardi R Júnior, Pimenta AM, et al. Exposure to an extremely low-frequency electromagnetic field only slightly modifies the proteome of Chromobacterium violaceumATCC 12472. Genet Mol Biol. 2015; 38(2):227-30. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
58. El May A, Snoussi S, Ben Miloud N, Maatouk I, Abdelmelek H, Ben Aïssa R, Landoulsi A. Effects of static magnetic field on cell growth, viability, and differential gene expression in Salmonella. Foodborne Pathog Dis. 2009; 6(5):547-52. DOI | PubMed
59. Mortazavi SMJ, Zarei S, Taheri M, Tajbakhsh S, Mortazavi SA, Ranjbar S, et al. Sensitivity to Antibiotics of Bacteria Exposed to Gamma Radiation Emitted from Hot Soils of the High Background Radiation Areas of Ramsar, Northern Iran. Int J Occup Environ Med. 2017; 8(2):80-4. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
60. Mortazavi SMJ, Darvish L, Abounajmi M, Zarei S, Zare T, Taheri M, Nematollahi S. Alteration of Bacterial Antibiotic Sensitivity After Short-Term Exposure to Diagnostic Ultrasound. Iran Red Crescent Med J. 2015; 17(11):e26622. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
61. Adebayo EA, Adeeyo AO, Ayandele AA, Omomowo IO. Effect of radiofrequency radiation from telecommunication base stations on microbial diversity and antibiotic resistance. JASEM. 2014; 18(4):669-74. DOI
62. Richter F. More Phones Than People. Statista; 2023. Available from: https://www.statista.com/chart/4022/mobile-subscriptions-and-world-population/
63. CDC. AR Threats Report. United States. 2019. Available from: https://www.cdc.gov/antimicrobial-resistance/data-research/threats/index.html
64. Pall ML. Wi-Fi is an important threat to human health. Environ Res. 2018; 164:405-16. DOI | PubMed
65. Barnes FS, Greenebaum B. Biological and medical aspects of electromagnetic fields. CRC Press; 2006.
66. WHO. Framework for developing health-based EMF standards. Geneva, Switzerland: World Health Organization; 2016.
67. Kostoff RN, Heroux P, Aschner M, Tsatsakis A. Adverse health effects of 5G mobile networking technology under real-life conditions. Toxicol Lett. 2020; 323:35-40. DOI | PubMed
68. Dörr T, Vulić M, Lewis K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 2010; 8(2):e1000317. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
69. Wood TK, Knabel SJ, Kwan BW. Bacterial persister cell formation and dormancy. Appl Environ Microbiol. 2013; 79(23):7116-21. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
70. Dörr T, Lewis K, Vulić M. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 2009; 5(12):e1000760. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
71. Cui P, Niu H, Shi W, Zhang S, Zhang W, Zhang Y. Identification of Genes Involved in Bacteriostatic Antibiotic-Induced Persister Formation. Front Microbiol. 2018; 9:413. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
72. Drlica K. The mutant selection window and antimicrobial resistance. J Antimicrob Chemother. 2003; 52(1):11-7. DOI | PubMed
73. Zhao X, Drlica K. Restricting the selection of antibiotic-resistant mutant bacteria: measurement and potential use of the mutant selection window. J Infect Dis. 2002; 185(4):561-5. DOI | PubMed
74. Mortazavi SMJ. Window theory in non-ionizing radiation-induced adaptive responses. Dose Response. 2013; 11(2):293-4. Publisher Full Text | DOI | PubMed [ PMC Free Article ]
75. Mitchel RE. The dose window for radiation-induced protective adaptive responses. Dose Response. 2009; 8(2):192-208. Publisher Full Text | DOI | PubMed [ PMC Free Article ]