Evaluation of the 900 MHz Radiofrequency Radiation Effects on the Antimicrobial Susceptibility and Growth Rate of Klebsiella pneumoniae


avatar Mohammad Taheri 1 , avatar Mohammad Moradi 1 , * , avatar SMJ Mortazavi 2 , 3 , avatar Shahla Mansouri 1 , avatar Gholamreza Hatam 4 , avatar Fatemeh Nouri 5

Department of Microbiology, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran
Ionizing and Non-Ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences, Shiraz, Iran
Medical Physics and Medical Engineering Department, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
Basic Sciences in Infectious Diseases Research center, Shiraz University of Medical Sciences, Shiraz, Iran
Department of Pharmaceutical Biotechnology, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

how to cite: Taheri M, Moradi M, Mortazavi S, Mansouri S, Hatam G, et al. Evaluation of the 900 MHz Radiofrequency Radiation Effects on the Antimicrobial Susceptibility and Growth Rate of Klebsiella pneumoniae. Shiraz E-Med J. 2017;18(3):e44946. https://doi.org/10.17795/semj44946.



Drug resistance to one or more antibiotics is mainly believed to be a serious threat to global public health which occurs by various mechanisms. The electromagnetic field as a nonchemical tool is capable of altering the antimicrobial susceptibility of bacteria. The aim of this study is the evaluation of the antimicrobial susceptibility of the Klebsiella pneumoniae to antibiotics before and after exposure to 900 MHz radiofrequency (RF) radiation produced by a mobile phone.


Antimicrobial susceptibility of the bacteria to antibiotics disks were performed after exposure to 900 MHz radiofrequency radiation. Antimicrobial susceptibility was carried out by Kirby-Bauer and the inhibition zone of each antibiotic disk was measured (as mean). Additionally, growth variations under exposure were recorded and an outgrowth curve was drawn.


Based on the results, after 12 hours of exposure to 900MHz radiofrequency, there was observed a maximum increase in the sensitivity of K. pneumoniae and shown that radiofrequency (RF) radiation can change antimicrobial sensitivity significantly (P < 0.05). Also, the radiofrequency radiation effect on the bacterial proliferation was evaluated and showed that exposure enables the bacteria to grow faster in the exponential phase than the non-exposed bacteria.


The findings of the study indicated that the sensitivity of K. pneumoniae was significantly increased to the various antibiotics after 12 hours of exposure to 900 MHz radiofrequency radiation. These observations could be interpreted by the concept of non-linearity in the responses of K. pneumoniae to different antibiotics after exposure to electromagnetic radiofrequency radiation and can be useful in the management of serious infectious diseases.

1. Introduction

Klebsiella pneumoniae is a member of the Klebsiella genus of Enterobacteriaceae. It is found in the normal flora of mouth, skin, and intestine. Nowadays, Klebsiella species are known as part of the important nosocomial pathogens. Most common infection caused by Klebsiella spp. is pneumonia, which usually causes bronchopneumonia (1). The rate of mortality is about 50% or more and even by antimicrobial treatment (2).

Electromagnetic irradiations are able to have an influence on bacteria and enhance (3) or inhibit (4) the bacterial growth rate. Extremely low-frequency magnetic fields can cause accumulation of the intracellular minerals such as calcium (5, 6). Calcium ions (Ca2+) are essential in the membrane for ATPases activity that provides energy for efflux pumps and ion channels (7). The intrinsic resistance to antibiotic substances is essential because of the efflux pumps that enables bacteria to stay alive in the presence of these toxic agents (8, 9).

Electromagnetic fields (EMFs) are also able to cause acute and chronic effects on the cells by increasing intracellular free radical levels. The free radicals can damage DNA and develop harmful cellular responses (6, 10). Several studies showed that EMFs could be applied as an antibacterial agent and also utilize as a nonchemical agent for healing or injuring the cells (11-13).

It is well known that physicochemical agents such as EMFs might be directly affected by bacterial growth and the bacteria are able to respond to the environmental stressors (14, 15). Several studies have demonstrated that EMFs can induce changes in bacterial morphology (16), antimicrobial susceptibility (17), proliferation, growth rate (18), and DNA repair (19).

Today, antibiotic resistance of bacteria is increasing due to overuse of antibiotics in chemotherapy, food source, agriculture, and animal husbandry (20-23). Bacterial resistance to one or more antibiotics occurs by various mechanisms (24-26). In this way, EMFs as an environmental agent could influence cellular responses such as antimicrobial susceptibility through different pathways (4, 20, 22, 23, 27). The aim of the present study was to evaluate the antimicrobial susceptibility of K. pneumoniae under 900 MHz radiofrequency radiations condition.

2. Methods

2.1. Antimicrobial Susceptibility Test

In this study, Klebsiella pneumoniae was isolated from the urine culture of the patients and identified in Shahid Faghihi hospital, Shiraz, Iran through conventional biochemical methods and confirmed by API protocol. The pure culture of K. pneumoniae was diluted in Mueller-Hinton Broth and reached 0.5 McFarland turbidity standard to get 1.5 × 108 CFU/mL as the total count (28). The bacterial suspension was spread on Mueller-Hinton agar (MHA-Biolife, Italy) plates and cultured with a set of antibiotics. They were tested by the disk diffusion method (Kirby-Bauer method) according to the clinical and laboratory standards institute guidelines (CLSI, 2013) that was conducted in the medical microbiology of Shiraz University of Medical Sciences. The incubation period was 18 - 24 hours at 35°C, then inhibition zone diameters for each antibiotic were measured.

2.2. Antimicrobial Agents

The antibiotics used were Imipenem (IMI 10 μg), Aztreonam (AZT 30 μg), Cefotaxime (CTX 30 μg), Piperacillin (PIPRA 100 μg), and Ceftriaxone (CTR 30 μg). (ROSCO Diagnostica DK-2630 Taastrup, Denmark). The results of antibiotic susceptibility tests pre and post exposure to 900 MHz radiation produced by RF simulator, were measured and analyzed. The inhibition zone of each antibiotic disk was recorded as mean in millimeter (mm). Three replicate agar plates were used for each regime (17).

2.3. RF Simulator

In this study, all exposures were performed using a GSM (900 MHz) mobile simulator (designed by department of medical physics and biomedical engineering, Shiraz, Iran) operating in the “Talk mode” and simulates the real condition of mobile phone radiation during calling. The radiofrequency (RF) simulator operated on the specific absorption rate (SAR) at the distance of 10 cm of the bacterial suspension (29).

2.4. Outgrowth Curve

The effects of radiofrequency exposure on the growth rates of bacteria were also investigated. The specified concentration of bacterial suspension inoculated in the broth medium precisely and then divided into 2 sets as a non-exposed (control) and the radiofrequency (RF) simulator exposed groups. For estimating the number of bacterial cells in a broth medium, the turbidity of each group was measured using optical density (OD) in 625 nm absorption (30) at different times by a spectrophotometer (UNICO UV-2100).

2.5. Statistical Analysis

All experiments were replicated 3 times for exposed and non-exposed groups. The means were compared using the non-parametric Mann-Whitney and t-test using SPSS 15 (P < 0.05).

3. Results

In the current study, antimicrobial susceptibility results of K. pneumoniae to 5 commonly antibiotics after exposure to 900 MHz radiofrequency radiation, for exposed and non-exposed (control) bacteria were summarized in Table 1. Furthermore, the effect of radiofrequency (RF) radiations on the growth rate of the bacteria was evaluated and the results for exposed and non-exposed bacteria were presented in Table 2. During exposure to radiofrequency radiation, the antimicrobial sensitivity of the bacteria was changed, but on the 12th hour of exposure, the sensitivity of the bacteria increased significantly (P < 0.05).

Table 1.

Inhibition Zone Diameters Before and After Exposure to RF Radiation for K. pneumoniaea

RF Simulator
Exposure TimeDrugControlExposureP Value
3hAZT26 ± 025.6 ± 0.580.2983
CTR24.6 ± 0.5824.6 ± 0.581.0000
IMI24.3 ± 0.5823.6 ± 0.580.2134
PIPRA25.3 ± 0.5824.6 ± 0.580.2134
CTX25.3 ± 0.5826.6 ± 0.580.0516
6hAZT26 ± 025 ± 00.0001*
CTR24.6 ± 0.5825 ± 00.2983
IMI24.3 ± 0.5826 ± 00.0071*
PIPRA25.3 ± 0.5823.6 ± 0.580.0230*
CTX25.3 ± 0.5826.6 ± 0.580.0516
12hAZT26 ± 030.3 ± 0.580.0002*
CTR24.6 ± 0.5829.3 ± 0.580.0006*
IMI24.3 ± 0.5825.6 ± 0.580.0516
PIPRA25.3 ± 0.5827.6 ± 0.580.0083*
CTX25.3 ± 0.5829.6 ± 0.580.0008*
18hAZT26 ± 025.6 ± 0.580.2983
CTR24.6 ± 0.5823.6 ± 0.580.1023
IMI24.3 ± 0.5825.6 ± 0.580.0516
PIPRA25.3 ± 0.5825.3 ± 0.581.0000
CTX25.3 ± 0.5824.6 ± 0.580.2134
24hAZT26 ± 025.6 ± 0.580.2983
CTR24.6 ± 0.5824.6 ± 0.581.0000
IMI24.3 ± 0.5824.3 ± 0.581.0000
PIPRA25.3 ± 0.5825.3 ± 0.581.0000
CTX25.3 ± 0.5825.3 ± 0.581.0000
Table 2.

Average Optical Density625 Results of K. pneumoniae Before and After Exposure

Experimental Results
TimeK. pneumoniae
ControlExposureP Value
0h0.005 ± 0.0010.006 ± 0.00050.196
1h0.01 ± 0.0010.013 ± 0.0010.0213*
2h0.03 ± 0.0010.04 ± 0.0010.0003*
3h0.28 ± 0.0010.37 ± 0.0020.0001*
4h0.38 ± 0.0010.34 ± 0.0010.0001*
5h0.35 ± 0.0020.33 ± 0.0020.0003*
6h0.37 ± 0.0020.34 ± 0.0010.0001*
7h0.35 ± 0.0020.34 ± 0.0020.0036*
8h0.34 ± 0.0010.34 ± 0.0010.9999
9h0.33 ± 0.0030.34 ± 0.0010.0054*
10h0.32 ± 0.0010.34 ± 0.0020.0001*
11h0.32 ± 0.0030.34 ± 0.0010.0004*
12h0.32 ± 0.0030.34 ± 0.0020.0007*
24h0.317 ± 0.0010.34 ± 0.0030.0002*

According to Table 1, it is clear that 900 MHz radiation has altered the antimicrobial susceptibility of the bacteria, which may be due to changes in their physicochemical properties. Hence, inhibition zone diameters of the pre and post exposed bacteria, for each antibiotic were measured and showed variations at different time exposure. As shown in Figure 1, there were no significant changes in sensitivity of the bacteria after 3rd and 6th hour, however, after exposure to the 12th hour, a maximum significant rise in the antibacterial sensitivity of the bacteria was observed. At the 18th and 24th hour exposure, the sensitivity of the bacteria to all antibiotics was decreased and bacteria tend to return to the early condition. Also, the effects of 900 MHz radiofrequency radiation on the growth rate of bacteria was carried out (Figure 2). Based on the bacteria that were exposed to radiation showed faster growth rate in exponential phase compared to bacteria in non-exposed groups. Moreover, the time to reach the logarithmic phase in the growth curve of the bacteria was faster in exposed groups.

Inhibition Zone Diameters Pre and Post Exposure to RF Simulator Radiation for K. pneumoniae
Inhibition Zone Diameters Pre and Post Exposure to RF Simulator Radiation for K. pneumoniae
Growth Curves of K. pneumoniae Before and After Radiation
Growth Curves of K. pneumoniae Before and After Radiation

4. Discussion

Results of the current study are in accordance with the previous study and similar studies on the effects of radiofrequency on the antimicrobial susceptibility of the K. pneumoniae after exposure to 2.4 GHz Wi-Fi radiofrequency radiation and supports the "window" theory concept (17, 31-36).

Based on this theory, when the irradiation level is within the window (between the lower and upper levels of the window), stimulatory effects of ionizing or non-ionizing radiation can be detected. Hence, the response of bacteria and other microorganisms to any environmental stressors can be determined by different field parameters such as the magnitude of the dose and dose rate. By comparison between this study and our previous study on K. pneumoniae response to radiofrequency radiation, the same pattern was repeated and showed a rise in antibacterial sensitivity within the window. However, for Wi-Fi exposure, this significant change was observed at 4.5 hours and for the RF simulator at the 12th hour. Many studies have demonstrated that the bacterial response to electromagnetic fields is dependent on several factors including: intensity, frequency, duration of exposure, and other physicochemical properties of the fields (22, 37, 38). As mentioned, the frequency of Wi-Fi router was 2.4 GHz and RF simulator was 900 MHz, maximum bacterial response to this radiation occurred at different times, which was related to their frequencies. Consequently, for Wi-Fi with higher frequency, this response was observed at 4.5 hours and for RF simulator with lower frequency, the same response was observed at the 12th hour.

We have also examined the effect of radiofrequency radiation on the growth rate of bacteria. As shown in Figure 2, during the investigated time period, K. pneumoniae showed a significant growth rate after exposure. However, several studies had indicated a fall in growth rate of bacteria depending on the field parameters for instance frequency, intensity, the magnitude of the field and exposure duration (20, 23). In another study on E. coli, growth rate decrease was more visible by 53 GHz radiation. Therefore, antibiotic susceptibility changes as a result of electromagnetic radiations (20). In one study (39) that demonstrated Low energy, low frequency radiation enhances the growth rate of microorganisms, although high-energy, high-frequency radiation kills the microorganisms.

The effects of electromagnetic fields on the biological systems are irrefutable. The modifications caused by irradiation have been usually considered as a harmful public concern. Hence, research on the probability of electromagnetic fields could be exploited for advantageous purposes.

Our findings of this study, on the antibacterial susceptibility of K. pneumoniae before and after exposure to 900 MHz RF radiation should be better considered in the treatment of the patients who suffer from the Klebsiella infections after additional investigations. Therefore, understanding the molecular mechanism involved in this response is very important. Previous studies on the bacterial sensitivity affected by electromagnetic fields were carried out and different mechanisms described this phenomenon:

a) Surface charges and membrane potential. Changes in membrane potential and surface charge, make disruption in the electron transport system and energy generation by proton motive force of bacteria would be impaired (40-42) and can increase sensitivity to antibiotics (43). Since membrane potential was crucial for bacterial binary fusion, it can be interpreted that exposure to EMFs influences the behavior of bacteria in the environment (44).

b) Increased efficacy of the antibiotics can be described as a result of electromagnetic field interactions with water molecules in the aqueous environment (45). It is obvious that the electromagnetic field changes physicochemical properties and hydration ability of water molecules and solubility of the antibiotics in the surrounding area was changed (20, 23).

c) One of the factors that can influence antibacterial sensitivity is the cell wall structure of bacteria and peptidoglycan (PG) nature (3, 46, 47). In gram-positive bacteria, cell wall thickness is greater than that of gram negatives.

d) It was demonstrated that electromagnetic field induces permeability of the bacteria and cells remained permeable after exposure to an electromagnetic field at least for 9 minutes especially with 18 GHz (47).

e) Efflux pumps and ion channels located in the cell membrane play an important role in antibiotic uptake by the cell. Electromagnetic fields are capable of changing the channels and pumps and duration of opening time will increase (17, 48, 49).

f) The last factor that can have an influence on the sensitivity of bacteria in the electromagnetic condition is the antibiotic structure. Charge, size, or hydrophilicity of the antibiotics can alter after being exposed to electromagnetic fields (50).

4.1. Conclusions

The bacteria were capable of responding to environmental stresses by activating some specific systems such as ion channels, change via the membrane, and DNA repair system. Considering these results, we believed that mobile exposure can serve as physical methods to change the antibacterial susceptibility of the microorganisms. In this light, K. pneumoniae responds to 900 MHz radiofrequency radiation exposure, variously and significant changes were observed at the 12th hour of exposure. Considering the importance of infections, especially caused by K. pneumoniae, experiments on different bacterial strains with various electromagnetic fields should be performed in the future to better clarify these uncertainties.

4.2. Suggestions

In order to extend the findings of this study to the other population, further studies on the molecular mechanisms of the bacterial responses and working on the several pathogenic, gram positive and negative bacteria, different exposure sources and time exposure will be suggested.



  • 1.

    Ko WC, Paterson DL, Sagnimeni AJ, Hansen DS, Von Gottberg A, Mohapatra S, et al. Community-acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerg Infect Dis. 2002;8(2):160-6. [PubMed ID: 11897067]. https://doi.org/10.3201/eid0802.010025.

  • 2.

    Jong GM, Hsiue TR, Chen CR, Chang HY, Chen CW. Rapidly fatal outcome of bacteremic Klebsiella pneumoniae pneumonia in alcoholics. Chest. 1995;107(1):214-7. [PubMed ID: 7813281].

  • 3.

    Torgomyan H, Kalantaryan V, Trchounian A. Low intensity electromagnetic irradiation with 70.6 and 73 GHz frequencies affects Escherichia coli growth and changes water properties. Cell Biochem Biophys. 2011;60(3):275-81. [PubMed ID: 21229332]. https://doi.org/10.1007/s12013-010-9150-8.

  • 4.

    Tadevosyan H, Kalantaryan V, Trchounian A. Extremely high frequency electromagnetic radiation enforces bacterial effects of inhibitors and antibiotics. Cell Biochem Biophys. 2008;51(2-3):97-103. [PubMed ID: 18633580]. https://doi.org/10.1007/s12013-008-9020-9.

  • 5.

    Ming-Yan L, Kun S, Xu Z, Imshik L. Mechanism for Alternating Electric Fields Induced-Effects on Cytosolic Calcium. Chinese Phys Lett. 2009;26(1):17102. https://doi.org/10.1088/0256-307x/26/1/017102.

  • 6.

    Montagnier L, Aissa J, Ferris S, Montagnier JL, Lavallee C. Electromagnetic signals are produced by aqueous nanostructures derived from bacterial DNA sequences. Interdiscip Sci. 2009;1(2):81-90. [PubMed ID: 20640822]. https://doi.org/10.1007/s12539-009-0036-7.

  • 7.

    Martins A, Machado L, Costa S, Cerca P, Spengler G, Viveiros M, et al. Role of calcium in the efflux system of Escherichia coli. Int J Antimicrob Agents. 2011;37(5):410-4. [PubMed ID: 21419607]. https://doi.org/10.1016/j.ijantimicag.2011.01.010.

  • 8.

    Davin-Regli A, Pagès JM. Regulation of efflux pumps in Enterobacteriaceae: genetic and chemical effectors. Antimicrob Resist Bacteria. 2006:55-75.

  • 9.

    Nikaido H. Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria. Seminars in cell & developmental biology. Elsevier; 2001. p. 215-23.

  • 10.

    Simko M, Mattsson MO. Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: possible immune cell activation. J Cell Biochem. 2004;93(1):83-92. [PubMed ID: 15352165]. https://doi.org/10.1002/jcb.20198.

  • 11.

    Yadollahpour A, Jalilifar M. Electromagnetic Fields in the Treatment of Wound: A Review of Current Techniques and Future Perspective. J Pure Appl Microbiol. 2014;8(4):2863-77.

  • 12.

    Androjna C, Fort B, Zborowski M, Midura RJ. Pulsed electromagnetic field treatment enhances healing callus biomechanical properties in an animal model of osteoporotic fracture. Bioelectromagnetics. 2014;35(6):396-405. [PubMed ID: 24764277]. https://doi.org/10.1002/bem.21855.

  • 13.

    Aziz Z, Cullum N, Flemming K. Electromagnetic therapy for treating venous leg ulcers. Cochrane Database Syst Rev. 2013;(2):CD002933. [PubMed ID: 23450536]. https://doi.org/10.1002/14651858.CD002933.pub5.

  • 14.

    Potenza L, Ubaldi L, De Sanctis R, De Bellis R, Cucchiarini L, Dacha M. Effects of a static magnetic field on cell growth and gene expression in Escherichia coli. Mutat Res. 2004;561(1-2):53-62. [PubMed ID: 15238230]. https://doi.org/10.1016/j.mrgentox.2004.03.009.

  • 15.

    Strasak L, Vetterl V, Fojt L. Effects of 50 Hz magnetic fields on the viability of different bacterial strains. Electromagnet Biol Med. 2005;24(3):293-300.

  • 16.

    Inhan-Garip A, Aksu B, Akan Z, Akakin D, Ozaydin AN, San T. Effect of extremely low frequency electromagnetic fields on growth rate and morphology of bacteria. Int J Radiat Biol. 2011;87(12):1155-61. [PubMed ID: 21401315]. https://doi.org/10.3109/09553002.2011.560992.

  • 17.

    Taheri M, Mortazavi SM, Moradi M, Mansouri S, Nouri F, Mortazavi SA, et al. 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. [PubMed ID: 26396967].

  • 18.

    Tessaro LW, Murugan NJ, Persinger MA. Bacterial growth rates are influenced by cellular characteristics of individual species when immersed in electromagnetic fields. Microbiol Res. 2015;172:26-33. [PubMed ID: 25721476]. https://doi.org/10.1016/j.micres.2014.12.008.

  • 19.

    Phillips JL, Singh NP, Lai H. Electromagnetic fields and DNA damage. Pathophysiology. 2009;16(2-3):79-88. [PubMed ID: 19264461]. https://doi.org/10.1016/j.pathophys.2008.11.005.

  • 20.

    Torgomyan H, Trchounian A. Escherichia coli membrane-associated energy-dependent processes and sensitivity toward antibiotics changes as responses to low-intensity electromagnetic irradiation of 70.6 and 73 GHz frequencies. Cell Biochem Biophys. 2012;62(3):451-61. [PubMed ID: 22101511]. https://doi.org/10.1007/s12013-011-9327-9.

  • 21.

    Xu C, Lin X, Ren H, Zhang Y, Wang S, Peng X. Analysis of outer membrane proteome of Escherichia coli related to resistance to ampicillin and tetracycline. Proteomics. 2006;6(2):462-73. [PubMed ID: 16372265]. https://doi.org/10.1002/pmic.200500219.

  • 22.

    Torgomyan H, Tadevosyan H, Trchounian A. Extremely high frequency electromagnetic irradiation in combination with antibiotics enhances antibacterial effects on Escherichia coli. Curr Microbiol. 2011;62(3):962-7. [PubMed ID: 21079961]. https://doi.org/10.1007/s00284-010-9811-2.

  • 23.

    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. [PubMed ID: 22667685]. https://doi.org/10.3109/1040841X.2012.691461.

  • 24.

    Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev. 2001;65(2):232-60. second page, table of contents. [PubMed ID: 11381101]. https://doi.org/10.1128/MMBR.65.2.232-260.2001.

  • 25.

    Winkler ML, Papp-Wallace KM, Hujer AM, Domitrovic TN, Hujer KM, Hurless KN, et al. Unexpected challenges in treating multidrug-resistant Gram-negative bacteria: resistance to ceftazidime-avibactam in archived isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2015;59(2):1020-9. [PubMed ID: 25451057]. https://doi.org/10.1128/AAC.04238-14.

  • 26.

    Perron GG, Whyte L, Turnbaugh PJ, Goordial J, Hanage WP, Dantas G, et al. Functional characterization of bacteria isolated from ancient arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLoS One. 2015;10(3):e0069533. [PubMed ID: 25807523]. https://doi.org/10.1371/journal.pone.0069533.

  • 27.

    Bulgakova VG, Grushina VA, Orlova TI, Petrykina ZM, Polin AN, Noks PP, et al. [The effect of millimeter-band radiation of nonthermal intensity on sensitivity of Staphylococcus to various antibiotics]. Biofizika. 1996;41(6):1289-93. [PubMed ID: 9044624].

  • 28.

    Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 2008;3(2):163-75. [PubMed ID: 18274517]. https://doi.org/10.1038/nprot.2007.521.

  • 29.

    Yuksel M, Naziroglu M, Ozkaya MO. Long-term exposure to electromagnetic radiation from mobile phones and Wi-Fi devices decreases plasma prolactin, progesterone, and estrogen levels but increases uterine oxidative stress in pregnant rats and their offspring. Endocrine. 2016;52(2):352-62. [PubMed ID: 26578367]. https://doi.org/10.1007/s12020-015-0795-3.

  • 30.

    Ziaei-Darounkalaei N, Ameri M, Zahraei-Salehi T, Ziaei-Darounkalaei O, Mohajer-Tabrizi T, Bornaei L. AZDAST the new horizon in antimicrobial synergism detection. MethodsX. 2016;3:43-52. [PubMed ID: 27408829]. https://doi.org/10.1016/j.mex.2016.01.002.

  • 31.

    Mortazavi S, Mosleh-Shirazi M, Tavassoli A, Taheri M, Bagheri Z, Ghalandari R, et al. A comparative study on the increased radioresistance to lethal doses of gamma rays after exposure to microwave radiation and oral intake of flaxseed oil. Iran J Radiat Res. 2011;9(1):9-14.

  • 32.

    Mortazavi SMJ, Motamedifar M, Namdari G, Taheri M, Mortazavi AR, Shokrpour N. Non-linear adaptive phenomena which decrease the risk of infection after pre-exposure to radiofrequency radiation. Dose Response. 2014;12(2):dose-response. 12-055. Mortazavi.

  • 33.

    Mortazavi SMJ, Motamedifar M, Mehdizadeh AR, Namdari G, Taheri M. The Effect of Pre-exposure to Radiofrequency Radiations Emitted from a GSM Mobile Phone on the Suseptibility of BALB/c Mice to Escherichia coli. J Biomed Phys Engin. 2012;2(4 Dec).

  • 34.

    Mortazavi S. Window theory in non-ionizing radiation-induced adaptive responses. Dose Response. 2013;11(2):293-4. [PubMed ID: 23930108]. https://doi.org/10.2203/dose-response.12-060.Mortazavi.

  • 35.

    Lei C, Berg H. Electromagnetic window effects on proliferation rate of Corynebacterium glutamicum. Bioelectrochem Bioenerget. 1998;45(2):261-5.

  • 36.

    Martirosyan V. The effects of physical factors on bacterial cell proliferation. J Low Frequency Noise Vibrat Active Control. 2012;31(4):247-55.

  • 37.

    Belyaev IY, Shcheglov VS, Alipov YD, Polunin VA. Resonance effect of millimeter waves in the power range from 10‐19 to 3× 10‐3 W/cm2 on Escherichia coli cells at different concentrations. Bioelectromagnetics. 1996;17(4):312-21.

  • 38.

    Torgomyan H, Ohanyan V, Blbulyan S, Kalantaryan V, Trchounian A. Electromagnetic irradiation of Enterococcus hirae at low-intensity 51.8- and 53.0-GHz frequencies: changes in bacterial cell membrane properties and enhanced antibiotics effects. FEMS Microbiol Lett. 2012;329(2):131-7. [PubMed ID: 22288948]. https://doi.org/10.1111/j.1574-6968.2012.02512.x.

  • 39.

    Jankovic S, Milosev M, Novakovic M. The effects of microwave radiation on microbial cultures. Hospital Pharmacol Int Multidisciplinar J. 2014;1(2):102-8. https://doi.org/10.5937/hpimj1402102J.

  • 40.

    Polk C. Electric fields and surface charges induced by ELF magnetic fields. Bioelectromagnetics. 1990;11(2):189-201. [PubMed ID: 2242053].

  • 41.

    Volpe P, Cappelli G, Mariani F, Serafino A, Eremenko T. Macrophage sensitivity to static magnetic fields. Biol Effects EMFs. 2002;1:374-81.

  • 42.

    Fadel MA, Mohamed SA, Abdelbacki AM, El-Sharkawy AH. Inhibition of Salmonella typhi growth using extremely low frequency electromagnetic (ELF-EM) waves at resonance frequency. J Appl Microbiol. 2014;117(2):358-65. [PubMed ID: 24766529]. https://doi.org/10.1111/jam.12527.

  • 43.

    Lee S, Hinz A, Bauerle E, Angermeyer A, Juhaszova K, Kaneko Y, et al. Targeting a bacterial stress response to enhance antibiotic action. Proc Natl Acad Sci U S A. 2009;106(34):14570-5. [PubMed ID: 19706543]. https://doi.org/10.1073/pnas.0903619106.

  • 44.

    Strahl H, Hamoen LW. Membrane potential is important for bacterial cell division. Proc Natl Acad Sci U S A. 2010;107(27):12281-6. [PubMed ID: 20566861]. https://doi.org/10.1073/pnas.1005485107.

  • 45.

    Caubet R, Pedarros-Caubet F, Chu M, Freye E, de Belem Rodrigues M, Moreau JM, et al. A radio frequency electric current enhances antibiotic efficacy against bacterial biofilms. Antimicrob Agents Chemother. 2004;48(12):4662-4. [PubMed ID: 15561841]. https://doi.org/10.1128/AAC.48.12.4662-4664.2004.

  • 46.

    Oncul S, Cuce EM, Aksu B, Inhan Garip A. Effect of extremely low frequency electromagnetic fields on bacterial membrane. Int J Radiat Biol. 2016;92(1):42-9. [PubMed ID: 26514970]. https://doi.org/10.3109/09553002.2015.1101500.

  • 47.

    Nguyen TH, Shamis Y, Croft RJ, Wood A, McIntosh RL, Crawford RJ, et al. 18 GHz electromagnetic field induces permeability of Gram-positive cocci. Sci Rep. 2015;5:10980. [PubMed ID: 26077933]. https://doi.org/10.1038/srep10980.

  • 48.

    Segatore B, Setacci D, Bennato F, Cardigno R, Amicosante G, Iorio R. Evaluations of the Effects of Extremely Low-Frequency Electromagnetic Fields on Growth and Antibiotic Susceptibility of Escherichia coli and Pseudomonas aeruginosa. Int J Microbiol. 2012;2012:587293. [PubMed ID: 22577384]. https://doi.org/10.1155/2012/587293.

  • 49.

    Blair JM, Richmond GE, Piddock LJ. Multidrug efflux pumps in Gram-negative bacteria and their role in antibiotic resistance. Future Microbiol. 2014;9(10):1165-77. [PubMed ID: 25405886]. https://doi.org/10.2217/fmb.14.66.

  • 50.

    Ke YL, Chang FY, Chen MK, Li SL, Jang LS. Influence of electromagnetic signal of antibiotics excited by low-frequency pulsed electromagnetic fields on growth of Escherichia coli. Cell Biochem Biophys. 2013;67(3):1229-37. [PubMed ID: 23703661]. https://doi.org/10.1007/s12013-013-9641-5.