Open access peer-reviewed chapter - ONLINE FIRST

Efficacy of Radiations against Bacterial Biofilms

Written By

Salma Kloula Ben Ghorbal, Rim Werhani and Abdelwaheb Chatti

Submitted: January 21st, 2022 Reviewed: February 10th, 2022 Published: April 16th, 2022

DOI: 10.5772/intechopen.103653

Bacterial Biofilms Edited by Theerthankar Das

From the Edited Volume

Bacterial Biofilms [Working Title]

Dr. Theerthankar Das

Chapter metrics overview

17 Chapter Downloads

View Full Metrics


A biofilm has been defined as a community of bacteria living in organized structures at a liquid interface. Biofilms can colonize a wide range of domains, including essentially industrial sectors, different natural environments, and also biomedical environments. Bacteria in biofilms are generally well protected against environmental stresses and, as a consequence, are extremely difficult to eradicate. The current study was to investigate the efficacy of different radiations against bacterial biofilms on different surfaces. It was established that the majority of available treatments have proven less effective against pathogenic biofilms, compared to planktonic bacteria. Therefore, new biofilm treatment strategies are needed, including physical treatments such as radiations. UV LEDs offer new solutions to prevent biofilm formation on inaccessible surfaces, such as medical and food equipment and, potentially, sanitary facilities, to limit nosocomial infections, compared to continuous UV irradiation treatment. Moreover, the antimicrobial effectiveness of gamma irradiation is therefore guaranteed in the treatment of bacteria associated with a biofilm, compared to planktonic bacteria. However, limited studies have been conducted to evaluate the inactivation effect of low-energy X-rays on more resistant biofilm pathogens on food-contact surfaces.


  • biofilm
  • bacteria
  • UV
  • X-rays
  • gamma irradiation
  • efficacy

1. Introduction

Biofilms consist of structured communities of bacteria, embedded in a self-produced polymeric matrix and adherent to inert or living surfaces [1, 2, 3]. Biofilm mode of growth is an approach in microorganisms to survive harsh growth conditions. Most microorganisms such as Pseudomonas aeruginosa[4], Staphylococcus aureus[5], and Escherichia coli[6] favor a way of life where the bacterial population is attached to a support, named sessile state, rather than free and isolated in the environment, named planktonic state. The attachment to a surface is a “survival strategy” that allows the bacteria to settle and colonize an environment. This structure represents the normal way of life of a bacterium [7]. This way of life is of great interest for the bacteria since it gives them a resistance to different sources of stress to which planktonic bacteria are sensitive [1]. In effect, bacteria in biofilms are generally well protected against environmental stresses, antibiotics [8], disinfectants, and the host immune system [9] and as a consequence are extremely difficult to eradicate [10]. Therefore, biofilms constitute a protected mode of growth that allows survival in a hostile environment. This strength is essentially due to the biofilm matrix composed of numerous polysaccharides, proteins, and extracellular DNA (eDNA) which is crucial in biofilm structural integrity [11]. Although it is widely accepted that eDNA is released primarily by cell lysis, several studies have shown that other mechanisms of active secretion may coexist [12]. This implies that eDNA is an interesting target in the control of biofilms. Numerous studies have demonstrated that biofilm formation can be prevented by enzymatic degradation of eDNA by DNase [11]. It was reported for Campylobacter.jejunibiofilm-attached to stainless steel surfaces that degradation of eDNA by exogenous addition of DNase led to rapid biofilm removal and is likely to potentiate the activity of antimicrobial treatments and thus synergistically aid disinfection treatments, like radiations, antibiotics [13]. For UVC radiation, they target genomic DNA by forming thymidine dimers in RNA and DNA, which can interfere with transcription and replication and thus induce bacterial death [14]. For the extracellular DNA, the formation of thymidine dimers, following exposure to UVC, has no consequence on bacterial multiplication. Therefore, the presence of eDNA in the matrix can only increase the viscosity of the matrix and therefore continues to block the passage of radiation through the biofilm which limits the effectiveness of the radiations.


2. Surfaces colonized by biofilms

Biofilms can colonize a wide range of domains, including essentially industrial sectors, different natural environments (soil, sediment, etc.), and biomedical environments [15]. Many bacteria form clumps at the bottom of the containers. Then, they reach the surface of the liquid-type media. However, some bacteria such as Salmonella[16], E. coli, P. fluorescens,and Vibrio choleraproduce rigid or fragile pellicle structures at air-liquid interfaces [17]. Biofilm production by the colonization of the air interface can facilitate and contribute to gas exchange while enabling the acquisition of nutrients and water from the liquid phase. The biofilms at air-liquid interfaces can cause severe problems in industrial water systems [18].

In the medical sector, microbial adhesion resulting in biofilm formation on implanted medical devices is a common occurrence and can lead to serious illness and death [19]. Implanted medical devices like intravascular catheters, urinary catheters, pacemakers, heart valves, stents, and orthopedic implants, normally used for therapeutic purposes, can also be the source of real infectious risks when colonized by bacterial biofilms [20].


3. Biofilms treatment

The majority of available antibacterial treatments have shown their effectiveness against planktonic bacteria. However, these treatments have proven to be ineffective against pathogenic biofilms [21, 22], which are thousands of times more resistant to this type of treatment [23, 24, 25]. It is therefore difficult to eradicate biofilms effectively because of the phenomenon of biofilm recalcitrance [22]. Despite the importance of biofilm treatment either in the medical or environmental sectors, studies into the effectiveness of irradiation on biofilm-associated cells are lacking. Therefore, new biofilm treatment strategies are needed, including physical treatments such as radiations. This review presents an overview of bacterial biofilm development and seeks to highlight the efficacy of radiations against bacterial biofilms.

3.1 Continuous UVC irradiation treatment efficiency on biofilms

Though germicidal UV radiation is widely applied for disinfection of water and food from planktonic bacteria, it may also be used to prevent bacterial growth and colonization on surfaces, as biofilms, within engineered systems [26]. Moreover, the UVC-based method is to be of practical use for disinfection of catheters in the clinic, as they are the major sources of infection [27]. However, higher UV doses would be required to inactivate biofilm-bound bacteria than planktonic bacteria because the biofilm would provide some degree of protection from the effects of UVC irradiation [28].

Torkzadeh et al. [26] have developed an experimental device and method to ensure the growth of biofilms in the presence of UV radiation and to measure the resulting reduction in surface biofilm growth. Under optimal growth conditions and after 48 h of growth, the reduction of the bio-volume of the E. colisurface is about 95% by a UV intensity of 50.5 μW/cm2 at 254 nm, compared to the control biofilms. The UV intensity required for biofilm prevention was greater than that expected due to the UV dose–response of tested bacteria and the cumulative doses applied to the tested surfaces. This results indicate that biofilms can form even under irradiation conditions that should inactivate planktonic cells completely. This is probably due to the protective effects of colloidal material and microbial exudates, that form biofilm matrix.

In water and wastewater infrastructure, biofilms pose a real problem for disinfection. Until now, the majority of ultraviolet (UV) disinfection studies focus on planktonic bacteria, with limited attention given to UV irradiation of biofilms. Among the few outstanding studies, the study of Myriam et al. [29] focused on the study of UVC dose/biofilm production relationship for five P.aeruginosastrains, isolated from wastewater. The aim was to evaluate the impact of incremental UVC doses, up to 100−2, on the ability of Pseudomonasstrains to produce biofilm, knowing that the UV dose equal to 40−2 is the dose recommended for the disinfection of water in Europe and America. The results of this study showed that biofilm production presents a progressive increase in function of an increasing of exposure UVC dose until a threshold UV dose. Moreover, the values of threshold UV doses were different in relation with the response of each bacteria strain to UVC dose (dose/response). This may be explained by the fact that intraspecific difference showed in the UV dose/response relationship is probably dependent on several factors: the degree of DNA damage induced by UV, the speed of induction of DNA repair mechanisms for each tested bacteria. On the other hand, beyond the threshold, a progressive decrease in the production of biofilm correlated with the increase of UV dose was noticed. This decrease in biofilm production can be explained by the fact that the bacterial strains have received a lethal UV dose reducing bacterial sustainability by the accumulation of photoproducts surpassing the capability of bacteria DNA repair mechanisms allowing for consequent, a decrease of biofilm formation and the weakening of this resistant structure.

The UV treatment has evolved a lot since the development of UV light sources from the conventional mercury lamp to the light-emitting diode (LED). It was established that pulsed UV can be more effective than a continuous emitting mode to control biofilms. Moreover, adaptable UV LED is promising to control biofilms in the water distribution system, according to the review of [30]. Luo et al. [30] have, recently, demonstrated that pulsed UV can be more effective than a continuous emitting mode to control biofilms, on one side and that a selective combination of UV LED wavelengths allows targeting damaged biofilm components, on the other hand.

In the medical sector, an application of radiation treatment on catheters looks promising. In this context, the study of Jimmy Bak et al. [31], who proposed a method for disinfecting the inner surface of catheters biofilm, has demonstrated that mean killing rates were 89.6% for 0.5 min exposure, 98% for 2 min exposure, and 99% for 60 min exposure. About 99% of the cells were killed with a UVC dose of 15 kJ m−2. This dose, which is 100 to 1000 times higher than the lethal dose required for planktonic cells, is assumed to be the maximum dose necessary to avoid contamination of newly inserted catheters. The need for high doses to kill mature biofilm and the limited effect of currently available UVC light sources result in a relatively long treatment time of about 60 minutes, hence the need for new UV sources like UV LED.

Recently, Jimmy Bak et al. [31] have tested a newly developed UVC disinfection device, which can be connected to a Luer catheter hub, on polymer tubes contaminated with a wide range of either bacterium, including S. aureus, E. coli,and P. aeruginosaand fungi like Candida albicans. Their results have shown no viable counts after 2 min of radiation for bacteria. Whereas, Killing of C. albicansneeds more than 20 minutes to be obtained in a UVC absorbing suspension.

On any type of surface contaminated by biofilm, the effectiveness of UVC light in inactivating biofilm-forming microorganisms is mainly due to the ability of DNA molecules to absorb UV photons between 200 and 300 nm, with an absorption peak at 260 nm, at first. Then, this uptake causes damage to the DNA by altering the pairing of nucleotide bases, creating new bonds between adjacent nucleotides on the same DNA strand. This damage occurs particularly between pyrimidine bases [32]. Therefore, to limit UV damages, bacteria generally possess molecular mechanisms to restore DNA lesions [33], which preserve the irradiated biofilm, from damage due to UVC exposure. This repair mechanism has been shown to be effective up to a threshold dose-related to a maximum accumulation of photoproducts and of reactive oxygen species, which can no longer be managed by this mechanism [29]. Our study in 2016, confirmed the oxidative stress through ROS accumulation, following UVC exposure, and has demonstrated that, in the enzymatic ROS-scavenging pathways, catalase and peroxidase enhancement improved the resistance of P. aeruginosatreated with incremental UV-C doses. However, longer exposure to UV-C rays inhibited SOD activity. This result confirms that SOD cannot efficiently remove superoxide radicals that accumulated in cells of P. aeruginosaat longer irradiation time and further confirms the inability of the repair system besides the ROS-scavenging pathways to deal with photoproducts and ROS accumulation, respectively [34, 35].

We can then conclude that the resistance of bacteria to UVC treatment remains at dose limits. Beyond these doses, there is an exhaustion of the repair system and a sure bacterial death. Hence the need to exceed the dose limits in order to escape bacterial resistance (Figure 1).

Figure 1.

UVC time/biofilm production relationship and DNA repair mechanisms.

3.2 UV LED irradiation treatment efficiency on biofilms

UV LEDs are emerging as competitive light sources because of advantages such as the possible selection of combined-wavelength UV LED [30], adjustable emitting mode, and the designable configuration that facilitate their incorporation into confined spaces. Therefore, UV LEDs offer new solutions to prevent biofilm formation on inaccessible surfaces, such as medical and food equipment and, potentially, sanitary facilities, to limit nosocomial infections. These results imply that surfaces more exposed to bacterial colonization require adequate UVC irradiation to prevent biofilm establishment. Furthermore, continuous surface irradiation may be insufficient as a sole source for biofilm prevention in many circumstances [26]. However, problems with low wall plugs and reliable power supplies still limit the effectiveness of UV LEDs, which further enlightens the prospective of UV in dealing with the biofilm issue in water infrastructure and also in the medical sector.

In this context, the study of Aikaterini et al. [36] on P. aeruginosabiofilms at different growth stages, within 24, 48, and 72 h of growth, was conducted to judge the effectiveness of ultraviolet B (UVB), at 296 nm and ultraviolet C (UVC) irradiation, with central wavelength at 266 nm, two different light-based treatments. The effectiveness of the UVB and UVC irradiations was quantified by counting colony-forming units. For UV exposure, a type of AlGaN light-emitting diodes (LEDs) was used to distribute UV irradiation on the biofilms. For P.aeruginosabiofilms, it appears that UVB irradiation is much more effective than UVC radiation for the inactivation of mature biofilms. The fact that UVB at 296 nm is present in daylight and has such a disinfecting capacity on biofilms opens the way to the treatment of infectious pathologies [36].

In parallel, the study of Gora et al. [37] has demonstrated that UV LED irradiation at 265 nm achieved 1.3 log inactivation of biofilm-bound P. aeruginosaat a UV dose of 8 mJ/cm2. This inactivation level is lower than those that have been reported by researchers using UVC LEDs to inactivate planktonic P. aeruginosa, a finding that can be explained by the higher resistance of biofilm-bound bacteria to UV inactivation.

Moreover, the combination of UV LED and Blue laser was tested on S. aureusbiofilm and gave the highest biofilm reduction of about 80.57%. It was then demonstrated that it to be the best choice to eradicate more biofilm [38].

Concerning the effect of radiations on biofilm matrix, it is well established that bacteria enclosed in a layer of exopolysaccharides are protected by 13% from UVC radiation. It was also confirmed that absorption of UV light by the alginate, an important matrix molecule, translated into a higher survival rate than observed with planktonic cells, for the same UV dose [39]. In effect, alginate water retention seems to be at the origin of the obvious ability to survive severe environments, like UVC exposure. On the other hand, the effect of UV LED on exopolysaccharides (EPS) has not been extensively studied, but it is predicted to be similar to the effect of continuous UVC on EPS. It is then assumed that following the prolonged exposure to UVC radiation, the production of EPS is stimulated [34]. Moreover, in the framework of the development of a profitable strategy to improve the EPS yield, UV irradiation mutagenesis of Bacillus licheniformissignificantly improved the EPS yield. Significantly enhanced yield (>3-folds) of EPS after UVC exposure can only confirm the stimulating effect of UVC radiation on the production of EPS, to ensure better protection against UVC rays and then bacterial survival [40] (Table 1).

Light sourcesMicroorganismsUV doseInactivationReference
UV LEDBiofilm-bound P.aeruginosa8 mJ/cm2 (265 nm)1.3 log reductionGora et al. [37]
Less mature P. aeruginosabiofilms (24 h grown)72–10,000 J∕m21 log
Aikaterini et al. [36]
Mature biofilms (48 and 72 h grown)20 000 J∕m20.8 _ 0.3 log reductions
Continuous low-intensity UVC irradiationE. coli50.5 μW/cm2 (254 nm)95%Torkzadeh et al. [26]
Catheter biofilm15 kJ/m299%Bak et al. [2731]
Wastewater40 mJ/cm2

Table 1.

UV doses required for the treatment of biofilms for different microorganisms.

3.3 Ionizing radiation treatment efficiency on biofilms

Ionizing radiation is a non-thermal destruction technique that inactivates pathogens that may contaminate certain food products, by exposing them to irradiation sources such as high-energy X-rays at about 5 MeV, gamma rays at about 2.5 MeV, or electron beams at about 10 MeV [41]. Compared to these conventional high-energy irradiation techniques, low-energy X-rays have a higher linear energy transfer (LET) value, resulting in a greater relative biological effect (RBE)[42]. Some previous studies have shown that low-energy X-rays is effective in destroying certain planktonic germs such as E. coliO157:H7, Salmonella, Listeria monocytogenes,and Shigella flexneri[43, 44, 45]. However, few studies have investigated the effect of low-energy X-rays on more resistant pathogens in mono-microbial or poly-microbial cultured biofilms and on food contact surfaces.

Despite of this, we could not simply conclude that low-energy X-rays destroyed EPS in biofilm. Therefore, we could at least postulate that low-energy X-rays irradiation weakened EPS structure in biofilm. Typical EPS mainly comprises homopolymers like cellulose and dextran and heteropolymers of alginate, emulsan, gellan, and xanthan, which maintain the stability of the biofilm matrix [46]. Ionizing irradiation can break down glycosidic bonds and consequently degrade polysaccharides and destabilize the biofilm [47].

Similarly, some in vitro studies also showed that the direct effect of radiation on oral C. albicanscells leads to a rapid proliferation ability, increase of virulent factors, and resistance to drugs [48]. Moreover, irradiated Klebsiella oxytocastrains of oral origin were more virulent than non-irradiated ones [49]. All of these results indicated that direct exposure of X-rays can affect the virulence of oral bacteria microbes even at therapeutic doses [50].

Concerning gamma irradiation, it is an established technology of well-documented safety and efficacy for the inactivation of pathogenic microorganisms such as Salmonella[51, 52]. Recently, gamma-ray sterilization was proven to be a viable method of sterilization of conducting polymer-based biomaterials for biomedical applications [53].

The study of [54] has demonstrated that in bacterial biofilms attached to stainless steel, gamma irradiation at a dose of 10.0 kGy reduced the counts of S. aureusattached for 1 hr. and overnight by ≥5.1 and 5.0 log CFU/cm2, respectively. Gamma irradiation at a dose of 1.0 kGy reduced the counts of P. aeruginosacounts to below the limit of detection (<2logCFU/cm2).

Concerning food sterilization, Salmonellais a problematic bacterium due to its biofilm resistance to chemical sanitizing treatments. Ionizing radiation is known to be used to inactivate Salmonellaon a variety of foods and contact surfaces in the food industry. The relative efficacy of the process against biofilm-associated cells versus free-living planktonic cells was tested for three food-borne-illness-associated isolates of Salmonella, by by Niemira and Solomonet [55]. They demonstrated that the dose of radiation required to reduce 90% (D10 values) of Salmonella entericaserovar Anatumwas not significantly different between biofilm-forming bacteria (0.645 kGy) and planktonic cells (0.677 kGy). In contrast, biofilm-forming cells of S. entericaserovar Stanleywere significantly more sensitive to ionizing radiation, with a D10 of 0.531, than planktonic cells, with a D10 of 0.591 kGy. D10 values of S. entericaserovar Enteritidiswere similarly decreased for biofilm-associated cells (0.436 kGy) in comparison to planktonic cells (0.535 kGy). The anti-microbial efficiency of ionizing radiation is therefore guaranteed in the treatment of bacteria associated with a biofilm. Ben Miloud YahiaYahia [52] proposed that the biofilm-forming abilities could be reduced with temperature decrease and increasing gamma radiation doses (Table 2).

Light sourcesMicroorganismsDoseInactivationReference
Gamma irradiationBiofilm-bound S. aureusattached for 1 h10.0 kGy≥5.1 log CFU/cm2
5.0 log
Biofilm-bound S. aureusattached overnight5.0 log CFU/cm2
Biofilm-bound P. aeruginosa1.0 kGy<2 log CFU/cm2
Salmonella entericaserovar A0.645 kGy1 log[31]
S. enterica serovar Stanley0.531 kGy1 log
S. enterica serovar Enteritidis0.436 kGy1 log

Table 2.

Gamma irradiation and doses required for the treatment of biofilms for different microorganisms.


4. Conclusion

This study has demonstrated that ionizing and non-ionizing radiation effectively reduces the populations of both planktonic and biofilm-associated bacteria. However, biofilms are confirmed to be more difficult to eradicate and require enhanced doses for their eradication. It was also confirmed that radiation sensitivity is microorganism specific. Likewise, the influence on radiation sensitivity of the cultured state of the organism, between planktonic and biofilm-associated, is also isolate specific, confirmed for gamma-treated Salmonella. But also, the stage of biofilm growth seems to affect the effectiveness of radiations treatment, as confirmed for Pseudomonasand Staphylococcusbiofilms. In general, these results show that, in contrast to chemical antimicrobial treatments, the antimicrobial efficacy of radiation is preserved or enhanced when treating biofilm-associated bacteria, compared to planktonic cells.


  1. 1. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: A common cause of persistent infections. Science. 1999;284(5418):1318-1322
  2. 2. Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews. 2002;15(2):167-193
  3. 3. Hall-Stoodley L, Hu FZ, Gieseke A, Nistico L, Nguyen D, Hayes J, et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA. 2006;296(2):202-211
  4. 4. Gellatly SL, Hancock RE. Pseudomonas aeruginosa: New insights into pathogenesis and host defenses. Pathogenic Diseases. 2013;67:159-173. DOI: 10.1111/2049-632X.12033
  5. 5. Gordon RJ, Lowy FD. Pathogenesis of methicillinresistantStaphylococcus aureusinfection. Clinical Infectious Diseases. 2008;46:S350-S359. DOI: 10.1086/533591
  6. 6. Beloin C, Roux A, Ghigo JM.Escherichia colibiofilms. Current Topical Microbiology. 2008;322:249-289. DOI: 10.1007/978-3-540-75418-3_12
  7. 7. Klinger E, Bouchard S, Légeron P, Roy S, Lauer F, Chemin I, et al. Virtual reality therapy versus cognitive behavior therapy for social phobia: A preliminary controlled study. Cyberpsychology & Behavior. 2005;8(1):76-88
  8. 8. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. International journal of antimicrobial agents. 2010;35(4):322-332
  9. 9. Jensen PO, Givskov M, Bjarnsholt T, Moser C. The immune system vs.Pseudomonas aeruginosabiofilms. FEMS Immunology and Medical Microbiology. 2010;59(3):292-305
  10. 10. Burmølle M, Thomsen TR, Fazli M, Dige I, Christensen L, Homøe P, et al. Biofilms in chronic infections–a matter of opportunity–monospecies biofilms in multispecies infections. FEMS Immunology & Medical Microbiology. 2010;59(3):324-336
  11. 11. Okshevsky M, Regina VR, Meyer RL. Extracellular DNA as a target for biofilm control. Current Opinion in Biotechnology. 2015;33:73-80
  12. 12. Wu J, Xi C. Evaluation of different methods for extracting extracellular DNA from the biofilm matrix. Applied and Environmental Microbiology. 2009;75(16):5390-5395
  13. 13. Brown HL, Hanman K, Reuter M, Betts RP, Van Vliet AH.Campylobacter jejunibiofilms contain extracellular DNA and are sensitive to DNase I treatment. Frontiers in Microbiology. 2015;10(6):699
  14. 14. Pereira RV, Bicalho ML, Machado VS, et al. Evaluation of the effects of ultraviolet light on bacterial contaminants inoculated into whole milk and colostrum, and on colostrum immunoglobulin G. Journal of Dairy Science. 2014;97(5):2866-2875. DOI: 10.3168/jds.2013-7601
  15. 15. Bryers JD. Medical biofilms. Biotechnology and Bioengineering. 2008;100(1):1-8
  16. 16. Scher K, Romling U, Yaron S. Effect of heat, acidification, and chlorination onS. entericaserovar Typhimurium cells in a biofilm formed at the air-liquid interface. Applied and environmental microbiology. 2005;71(3):1163-1168
  17. 17. Armitano J, Méjean V, Jourlin-Castelli C. G ram-negative bacteria can also form pellicles. Environmental Microbiology Reports. 2014;6(6):534-544
  18. 18. Rühs PA, Böcker L, Inglis RF, Fischer P. Studying bacterial hydrophobicity and biofilm formation at liquid–liquid interfaces through interfacial rheology and pendant drop tensiometry. Colloids and Surfaces B: Biointerfaces. 2014;117:174-184
  19. 19. Habash M, Reid G. Microbial biofilms: Their development and significance for medical device-related infections. Journal of Clinical Pharmacology. 1999;39:887-898. DOI: 10.1177/00912709922008506
  20. 20. Francolini I, Donelli G. Prevention and control of biofilmbased medical-device-related infections. FEMS Immunology Medicine and Microbiology. 2010;59:227-238. DOI: 10.1111/j.1574-695X.2010.00665.x
  21. 21. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, et al. Bacterial biofilms in nature and disease. Annual Review of Microbiology. 1987;41:435-464. DOI: 10.1146/annurev.mi.41.100187.002251
  22. 22. Lebeaux D, Ghigo J-M, Beloin C. Biofilm-related infections: Bridging the gap between clinical management and fundamental aspectsof recalcitrance toward antibiotics. Microbiology and Molecular Biology Reviews. 2014;78:510-543. DOI: 10.1128/MMBR.00013-14
  23. 23. Davies D. Understanding biofilm resistance to antibacterial agents. Natural Review Drug Discovery. 2003;2:114-122. DOI: 10.1038/nrd1008
  24. 24. Luppens SBI, Reij MW, van der Heijden RWL, Rombouts FM, Abee T. Development of a standard test to assess the resistance ofS. aureusbiofilm cells to disinfectants. Applied Environmental Microbiology. 2002;68:4194-4200. DOI: 10.1128/AEM.68.9.4194-4200.2002
  25. 25. Stewart PS, andWilliam Costerton, J. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358:135-138. DOI: 10.1016/S0140-6736(01)05321-1
  26. 26. Torkzadeh H, Zodrow KR, Bridges WC, Cates EL. Quantification and modeling of the response of surface biofilm growth to continuous low intensity UVC irradiation. Water Research. 2021;1(193):116895
  27. 27. Bak J, Ladefoged SD, Tvede M, Begovic T, Gregersen A. Dose requirements for UVC disinfection of catheter biofilms. Biofouling. 2009;25(4):289-296
  28. 28. Da Silva Araújo, Paula Alexandra. Biofilm Control with Antimicrobial Agents: The Role of the Exopolymeric Matrix. Diss. Universidade do Porto (Portugal), 2014
  29. 29. Myriam BE, Khefacha S, Maalej L, Imen DA, Hassen A. Effect of ultraviolet, electromagnetic radiation subtype C (UV-C) dose on biofilm formation byPseudomonas aeruginosa. African Journal of Microbiology Research. 2011;5(25):4353-4358
  30. 30. Luo X, Zhang B, Lu Y, Mei Y, Shen L. Advances in application of ultraviolet irradiation for biofilm control in water and wastewater infrastructure. Journal of Hazardous Materials. 2022;421:126682
  31. 31. Bak J, Begovic T, Bjarnsholt T, Nielsen A. A UVC device for intra-luminal disinfection of catheters: In vitro tests on soft polymer tubes contaminated withPseudomonas aeruginosa,Staphylococcus aureus,Escherichia coliandCandida albicans. Photochemistry and Photobiology. 2011;87(5):1123-1128
  32. 32. Myriam BS, Otaki M, Shinobu K, Abdennaceur H. Detection of active E. coli after irradiation by pulsed UV light using a Q phage. African Journal of Microbiology Research. 2010;4(11):1128-1134
  33. 33. Rastogi RP, Kumar A, Tyagi MB, Sinha RP. Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. Journal of Nucleic Acids. 2010;2010:1-32
  34. 34. Kloula Ben Ghorbal S, Rim W, Abdelwaheb C. Role of Mn-cofactored superoxide dismutase in the aptitude of P. aeruginosa to form biofilm, under UV-C radiations. Journal of New Sciences, Agriculture and Biotechnology. 2022;88; article in press
  35. 35. Salma KB, Lobna M, Sana K, Kalthoum C, Imene O, Abdelwaheb C. Antioxidant enzymes expression inP. aeruginosaexposed to UV-C radiation. Journal of Basic Microbiology. 2016;56(7):736-740
  36. 36. Argyraki A, Markvart M, Bjørndal L, Bjarnsholt T, Petersen PM. Inactivation of Pseudomonas aeruginosa biofilm after ultraviolet light-emitting diode treatment: A comparative study between ultraviolet C and ultraviolet B. Journal of Biomedical Optics. 2017;22(6):065004
  37. 37. Gora SL, Rauch KD, Ontiveros CC, Stoddart AK, Gagnon GA. Inactivation of biofilm-bound Pseudomonas aeruginosa bacteria using UVC light emitting diodes (UVC LEDs). Water research. 2019;15(151):193-202
  38. 38. Astuti SD, Rasheed A, Rahmawati I, Puspita PS, Kholimatussa’diah S, Putra AP. Combination of blue laser exposure with UV-LED to improve antimicrobial effects onStaphylococcus aureusbiofilm. Malaysian Journal of Medicine and Health Sciences. 2020;16(S4):6-11
  39. 39. Elasri MO, Miller RV. Study of the response of a biofilm bacterial community to UV radiation. Applied and Environmental Microbiology. 1999;65(5):2025-2031
  40. 40. Asgher M, Urooj Y, Qamar SA, Khalid N. Improved exopolysaccharide production from Bacillus licheniformis MS3: Optimization and structural/functional characterization. International Journal of Biological Macromolecules. 2020;151:984-992
  41. 41. Zhang J, Xie Y, Li Y, Shen C, Xia Y. Covid-19 screening on chest x-ray images using deep learning based anomaly detection. 2020;27(27). arXiv preprint arXiv:2003.12338
  42. 42. Hill MA. The variation in biological effectiveness of X-rays and gamma rays with energy. Radiation Protection Dosimetry. 2004;112(4):471-481
  43. 43. Aleid SM, Dolan K, Siddiq M, Jeong S, Marks B. Effect of low‐energy X‐ray irradiation on physical, chemical, textural and sensory properties of Dates. International journal of food science & technology. 2013;48(7):1453-1459
  44. 44. Jeong H, Kim SH, Han SS, Kim MH, Lee KC. Changes in membrane fatty acid composition through proton-induced fabF mutation enhancing 1-butanol tolerance in E. coli. Journal of the Korean Physical Society. 2012;61(2):227-233
  45. 45. Moosekian SR, Jeong S, Ryser ET. Inactivation of sanitizer-injuredEscherichia coliO157: H7 on baby spinach using X-ray irradiation. Food Control. 2014;36(1):243-247
  46. 46. Svenningsen NB et al. The biofilm matrix polysaccharides cellulose and alginate both protect Pseudomonas putida mt-2 against reactive oxygen species generated under matric stress and copper exposure. Microbiology. 2018;164(6):883-888
  47. 47. Lembre P, Lorentz C, Di Martino P. Exopolysaccharides of the biofilm matrix: A complex biophysical world. The complex world of polysaccharides. 2012;31:371-392
  48. 48. Ueta E, Tanida T, Osaki T. A novel bovine lactoferrin peptide, FKCRRWQWRM, suppresses Candida cell growth and activates neutrophils. The Journal of Peptide Research. 2001;57(3):240-249
  49. 49. Vanhoecke BW, De Ryck TR, De Boel K, Wiles S, Boterberg T, Van de Wiele T, et al. Low-dose irradiation affects the functional behavior of oral microbiota in the context of mucositis. Experimental Biology and Medicine. 2016;241(1):60-70
  50. 50. Wang Z, Zhou Y, Han Q, Ye X, Chen Y, Sun Y, et al. Synonymous point mutation of gtfB gene caused by therapeutic X-rays exposure reduced the biofilm formation and cariogenic abilities ofStreptococcus mutans. Cell & Bioscience. 2021;11(1):1-3
  51. 51. Rezende AC, Igarashi MC, Destro MT, Franco BD, Landgraf M. Effect of gamma radiation on the reduction of Salmonella strains, Listeria monocytogenes, and Shiga toxin–producingEscherichia coliand sensory evaluation of minimally processed spinach (Tetragonia expansa). Journal of Food Protection. 2014;77(10):1768-1772
  52. 52. Ben Miloud Yahia N, Ghorbal SKB, Maalej L, Chatti A, Elmay A, Chihib NE, et al. Effect of temperature and gamma radiation on Salmonella Hadar biofilm production on different food contact surfaces. Journal of Food Quality. 2018
  53. 53. Kim S, Jeong JO, Lee S, Park JS, Gwon HJ, Jeong SI, et al. Effective gamma-ray sterilization and characterization of conductive polypyrrole biomaterials. Scientific Reports. 2018;8(1):1-10
  54. 54. Kim JH, Jo CR, Rho YT, Lee CB, Byun MW. Comparison of gamma irradiation and sodium hypochlorite treatments to inactivateStaphylococcus aureusandPseudomonas aeruginosabiofilms on stainless steel surfaces. Food Science and Biotechnology. 2007;16(2):315-319
  55. 55. Niemira BA, Solomon EB. Sensitivity of planktonic and biofilm-associated Salmonella spp. to ionizing radiation. Applied and Environmental Microbiology. 2005;71(5):2732-2736

Written By

Salma Kloula Ben Ghorbal, Rim Werhani and Abdelwaheb Chatti

Submitted: January 21st, 2022 Reviewed: February 10th, 2022 Published: April 16th, 2022