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Middle East African Journal of Ophthalmology Middle East African Journal of Ophthalmology
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  Table of Contents 
Year : 2021  |  Volume : 28  |  Issue : 2  |  Page : 116-122  

Multi-purpose disinfecting solutions only partially inhibit the development of ocular microbes biofilms in contact lens storage cases

1 Department of Molecular Biology, Curse of Post-Graduation in Cellular and Molecular Biology, CCEN, UFPB, João Pessoa, Brazil
2 Department of Biotechnology, Laboratory of Environmental Microbiology, CBIOTEC, UFPB, João Pessoa, Brazil
3 Department of Cellular and Molecular Biology, Laboratory of Biotechnology of Aquatic Organisms, CBIOTEC, UFPB, João Pessoa, Brazil

Date of Submission15-Sep-2020
Date of Acceptance14-Jul-2021
Date of Web Publication25-Sep-2021

Correspondence Address:
Dr. Ulrich Vasconcelos
Department of Biotechnology, Laboratory of Environmental Microbiology, CBIOTEC, UFPB João Pessoa
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/meajo.meajo_414_20

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PURPOSE: Certain ocular resident or pathogenic microbes may remain viable in the presence of multi-purpose disinfectant solutions (MPDSs), subsequently developing biofilms inside contact lens storage cases (CLSCs) which pose a risk of infection to wearers. This study evaluated the formation of ocular microbiota biofilms exposed to three top selling MPDS.
METHODS: Crystal violet assay was carried out for the verification of biofilm formation. The in vitro assays evaluated Pseudomonas aeruginosa UFPEDA 416 and Staphylococcus aureus UFPEDA 02 exposure of 48 h to MPDS, as well as the use of 40 KHz ultrasound at the beginning and with 24 h immersion in the MPDS. Subsequently, in vivo assays evaluated the formation of microbial biofilms on the CLSC walls containing silicone-hydrogel contact lenses immersed in MPDS from 15 healthy volunteer patients, who had been wearing the lenses for 7 days.
RESULTS: Biofilms were inhibited by 26%–98% in the in vitro assays, with a statistically significant difference only for P. aeruginosa UFPEDA 416 exposed to diluted MPDS. Most inhibitions occurred moderately and weakly. In addition, adherent cells were detected in more than 90% of the tests. Biofilm was not inhibited in more than one third of the results, nor was it disturbed, especially with the ultrasound treatments. The average of obtained optical densities at 590 nm was between 0.6 and 0.8 in the in vivo assays. The results were similar between the CLSC right and left wells. There was a correlation between microbial biofilm formation and the type of MPDS tested, with statistical difference between the three treatments.
CONCLUSION: MPDS promoted a partial inhibition of microbial biofilm formation but only one MPDS proved to be more effective in vitro and in vivo. This study, however, could not distinguish the effect of possible errors in the good hygiene practices of the users.

Keywords: Biofilms, eye care, Paraíba, Pseudomonas aeruginosa, Staphylococcus aureus

How to cite this article:
M. de Araújo FB, Morais VC, M. de Oliveira BT, G. de Lima KY, Gomes VT, G. do Amaral IP, Vasconcelos U. Multi-purpose disinfecting solutions only partially inhibit the development of ocular microbes biofilms in contact lens storage cases. Middle East Afr J Ophthalmol 2021;28:116-22

How to cite this URL:
M. de Araújo FB, Morais VC, M. de Oliveira BT, G. de Lima KY, Gomes VT, G. do Amaral IP, Vasconcelos U. Multi-purpose disinfecting solutions only partially inhibit the development of ocular microbes biofilms in contact lens storage cases. Middle East Afr J Ophthalmol [serial online] 2021 [cited 2022 Jun 25];28:116-22. Available from: http://www.meajo.org/text.asp?2021/28/2/116/326668

   Introduction Top

Soft contact lenses (SCLs) are ophthalmic orthoses widely used in ametropic individuals and provide better visual acuity in patients with myopia, hyperopia, astigmatism, and presbyopia. In addition, they offer the practicality and esthetic benefit of replacing glasses in everyday activities, such as sports and social life.[1] SCL also may have a therapeutic use, to protect the corneal surface.[2] Another associated benefit is the fact that these lenses are disposable after 30 days of use, a factor that directly contributes to the prevention of infectious complications related to prolonged use.[3]

Over the past five decades, contact lens wear has increased significantly worldwide.[4] The first contact lenses were made of rigid material and caused great discomfort during the use. However, the evolution of the materials used in the manufacture of SCL has facilitated the commercialization of highly comfortable silicone-hydrogel contact lenses, easy to maintain, clean, handle, and adapt. About 50%–75% of the prescribed SCL in the world are made from silicone-hydrogel material.[5]

Parallel to the evolution of contact lenses, the design of new formulations guaranteed the need for multi-purpose disinfection solutions (MPDS) employed for clean, rinse, disinfect, retain moisture and store the lenses.[6] However, improper handling and incorrect hygiene habits by wearers, such as overnight use of the lenses, may favor SCL contamination and colonization, as well as on the surfaces inside the contact lens storage cases (CLSC).[7] Both are important pathogen fomites related to eye infections in SCL wearers, especially the CLSC.[8],[9],[10],[11],[12]

The ocular surface is not a sterile environment. Resident conjunctival microbiota assists ocular surface integrity and homeostasis and may vary according to age and gender.[13] However, the use of SCL may alter the ocular surface microbiota and provoke risk of infections due to the expansion of surface for pathogen binding.[14]

MPDS are formulated to ensure wettability and lubrication.[5] Some of the components are efficient in protein reduction and lipid absorption.[15] The active substances in MPDS composition must have antimicrobial properties that can guarantee the safety of the product, especially against the two most common pathogens associated with eye infections: Pseudomonas aeruginosa and Staphylococcus aureus. Manufacturers recommend a minimum of 6 h contact with active MPDS agents to affect cell viability.[16] The effect of this is to disturb the microbial capacity for carrying out all cellular functions required for lens maintenance under normal living conditions.[17]

P. aeruginosa and S. aureus exhibit several virulence factors, particularly the ability to aggregate in biofilms.[18] Adhered to contact lens surfaces or CLSC walls, biofilms increase resistance to antimicrobial agents by 10–1000 times.[19] Thus, critical points regarding care during the use of SCL include lens care regimen, personal hygiene, and climatic factors.[20]

Although the antimicrobial activity of MPDS is expected and desired,[21] the efficacy of these products has not received absolute consensus and sometimes even questioned.[22],[23],[24] Given this, the aim of this study was to evaluate the formation of microbial biofilms on polystyrene surface exposed to three different brands of MPDS.

   Methods Top

Multi-purpose disinfecting solutions

Three solutions of the most consumed brands in North-east Brazil[25] were chosen, coded as MPDS-A, MPDS-B, and MPDS-C. Solution leaflets were evaluated for the identification of formulation components.

In vitro quantitative microtiter adherence assay

It was used the crystal violet assay with minor adaptations.[26] Briefly, 1.5 μL polystyrene microdilution tubes were filled with 800 μL of nutrient broth, 100 μL of MPDS, and 100 μL of suspended strains, P. aeruginosa UFPEDA 416 or S. aureus UFPEDA 02, whose suspensions were prepared with NaCl 0.85% (w/v) and turbidity standardized with the MacFarland #1 tube. For the comparison purposes, the strains were also inoculated in 100% MPDS.

After incubation (48 h at 37°C), the content of the microdilution tubes was discarded and the walls washed 3-5 times with distilled water to remove any deposited planktonic cells. The tubes were allowed to dry at the room temperature for 1 h. Afterward, 1.5 ml of the 1% crystal violet solution (Newprov, Brazil) was transferred, and 20 min later, the dye was discarded. The crystal violet excess was removed with distilled water and given another hour to dry at the room temperature. Then, 1.5 ml of 95% ethanol was added (Química Moderna, Brazil), and after 30 min rest, the optical density of the crystal violet-ethanol solution was measured at 590 nm (Shimadzu, UV-1601-1601 PC). The control of the test was performed with strains inoculated in nutrient broth.

Ultrasound effect on microbial adhesion and biofilm maturation.

Forty KHz ultrasound (RM Techno Brazil, CD-3800) was applied for 10 min under two conditions: samples at the beginning of the test and samples 24 h after incubation at 37°C. All samples were incubated for 48 h at the same temperature, and the protocol to determine the percentage of inhibition of cell adhesion to the conditioning substrate was conducted by the crystal violet assay.

Interpretation criteria

The percent inhibition of adhesion was calculated by the following formula: ([ODC-ODT] ÷ ODC) ×100, where ODC is the mean optical density of the control in nutrient broth and ODT is the average optical density of the treatment with the MPDS.[27] It was assumed that when ODT values exceeded 3ODC, they indicated the presence of adherent microbial cells.[28] In this study, the average cutoff was OD590 reading > 0.186. The classification of inhibition of biofilm formation followed the criteria proposed by a previous study,[29] considering as weak if <40%; moderate when >40 and <80%; or strong if >80%. The inhibition percentage equal to zero indicates that the mean ODT values were greater than ODC.

In vivo microbial adhesion assay in contact lens storage cases

Fifteen volunteer healthy patients were divided into three groups after signing an informed consent form approved by the ethics committee of the Health Sciences Center from the Universidade Federal da Paraíba (# 3.062.732, December 6, 2018). Each patient in each group received a kit containing an SCL (Acuvue® Oasys®, Johnson and Johnson), a sterile polystyrene case with side indicator cap (Pack lens, Brazil) and one brand of MPDS. All patients were instructed regarding good hygiene practices for lens handling, cleaning, maintenance, and packaging storage. The kits were kept at the room temperature and remained with the patients for 7 days, after which the CLSC was collected for the analysis. The contents of the cases were removed, and the crystal violet assay was conducted.

Statistical treatment

All the experiments were performed in triplicate. For the in vitro assays, the results were evaluated for the normal distribution by the Kolmogorov–Smirnov test. The mean difference between the groups was evaluated by the analysis of variance method. For in vivo assays, the Kolmogorov–Smirnov test was repeated and correlations between the variables were obtained by Spearman test, considering significant when P < 0.05.

   Results Top

Eighteen different substances were identified in the three MPDS. Using the Cosmetic Ingredient Review specifications,[30] six functions of these ingredients in the formulations were found: Preservative, chelating, surfactant, degenerating, lubricant, and buffering. Seven ingredients were found in all three solutions tested A, B, and C: Boric acid, disodium edetate, and sodium chloride. Three other ingredients were common only in solutions A and B: Poloxamin, sodium borate, and polyaminopropyl biguanide. One ingredient was only found in solutions B and C, polyquaternium 1. Of the five preservatives or disinfectants, boric acid was common to all three solutions while sodium borate and polyaminopropyl biguanide were common in two of the MPDS.

[Table 1] presents the results of the in vitro quantitative microtiter adherence assay. There were inhibitions of biofilm formation, but not under all conditions tested. Inhibitions found were classified as strong to moderate for both strains tested. The statistically significant difference occurred with P. aeruginosa UFPEDA 416 in the treatment with diluted MPDS (P < 0.01).
Table 1: Inhibition of the ocular pathogen adhesion over 48 h

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In only one treatment, there was a percentage of inhibition higher than 96% of biofilm formation, and adherent cells were absent: S. aureus UFPEDA 02 (MPDS-B) and P. aeruginosa UFPEDA 416 (MPDS-C). In the other treatments tested which include results around 75% of inhibition, these adherent cells remained present after 48 h of exposure to MPDS.

The 40 KHz ultrasound treatment favored the development of biofilms and did not promote disturbances of the mature biofilm. In addition, although ultrasound treatment at the beginning of the inoculation had reduced biofilm formation by 26%–60% (MPDS-A and B), this inhibition was from moderate to poor, and adherent cells were present.

The results from the in vivo microbial adhesion assay indicated a similar measurement of optical density in the right and left well samples. The correlation between biofilm formation and the type of MPDS tested reached between 62% and 79%. In addition, there was a statistical difference on microbial biofilm formation in the CLSC wells between the three treatments, highlighting MPDS-C as the solution with the lowest averages [Table 2]. During the in vivo assays, one of the patients declined to participate.
Table 2: Average* number of optical densities after 7 days of contact lens wearing and storage with different multiple-purpose disinfectant solutions

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[Figure 1] illustrates the similarity in biofilm formation on the surfaces inside the right and left wells of CLSC in all groups (Mean square = 0.385 and F = 11.189). This was found within each particular group (Mean square = 0.034), but was most distinctive for the group using MPDS-C.
Figure 1: Average biofilm formation in contact lens storage cases after 7 days of use by patients (harmonic mean size = 27.697)

Click here to view

   Discussion Top

Biofilms are sessile microbial communities consisting of one or more species living in close association, surrounded by an adhesive polymeric matrix.[31] A large number of bacteria can settle as aggregates and persist on the surfaces of different natures: Metals, ceramics, glass, and plastics. These materials, depending on their composition, can strongly support microbial growth over a long period of time and increase the risk of bacterial cross-contamination.[32]

Microbes remain irreversibly adhered to a surface and biofilms are the preferred form of microbial life on the earth.[33] Biofilms provide several advantages to their producers compared to planktonic phenotypes, in particular by ensuring greater resistance to environmental pressures, reduced susceptibility to antiseptics and other antimicrobial.[34] This characteristic feature can be attributed to the fact that they form and maintain multicellular communities involving complex mechanisms of cell signaling. The availability of nutrients plays the most important role in the events that culminate with the adhesion as well as the release of the cells.[35]

Ocular surface resident microbes are mostly commensal and not necessarily pathogenic. Lipids, proteins, and glycoproteins rapidly accumulate on the surfaces of a contact lens, thus favoring the adhesion of commensal bacteria and biofilm formation.[18] The CLSC may provide a particularly suitable survival niche for pathogens, contributing to their proliferation.[36]

The most frequently observed complications in contact lens wearers are: Inflammatory infiltrates, corneal ulcer, giant papillary conjunctivitis, and bacterial keratitis, which account for 25%–60% of complications in SCL wearers worldwide.[20] Furthermore, most contact lens wearers (over 80%) use SCL, which accounts for approximately 70% of cases of bacterial eye infections.[37]

P. aeruginosa is a pathogenic microorganism with clinical importance, associated with microbial keratitis.[38] The species along with S. aureus are the most prevalent bacteria in corneal infections associated with the wearing of contact lenses.[39] Eye diseases caused by S. aureus in wearers may be due to direct tissue invasion or virulence factors exhibited by the bacteria.[40]. Besides the risks related to the P. aeruginosa virulence profile, the bacterium can quickly colonize on the surface of a contact lens, using its physiological versatility, especially when some ocular inflammatory event is in progress. It is currently accepted that this phenomenon also occurs with other bacterial species.[41]

Cell adhesion on the conditioning substrate is determined by the equilibrium between van der Waals forces due to double-layer electrical interactions.[42] The nature of the surface also plays a key role. Hydrophobic surfaces, such as polystyrene, a common material found in the CLSC, as well as the microtubes used in the in vitro assays, have a water contact angle >65°. This reflects low Gibbs free energy, favoring the cell sorption.[43] The water contact angle on polystyrene surfaces can reach up to 90°.[44] Importantly, the adhesion of some isolates of P. aeruginosa and Staphylococcus sp. has been observed on the surfaces of different materials also considered hydrophobic but different from polystyrene, for example, stainless steel and rubber.[45]

MPDS are supposed to be effective in the four steps of contact lens treatment: Cleaning, rinsing, disinfecting, and storage. As effective as the disinfectant action of the solutions may be, it only partially inhibits the formation of biofilms of ocular microbes, as was observed in this study. In the in vitro assays, biofilms formed by P. aeruginosa UFPEDA 416 were slightly more susceptible than those formed by S. aureus UFPEDA 02. In 33% of the assays, however, biofilm inhibition was zero. More importantly, in a significant majority of assays, adherent cells were found, guaranteeing the formation and maintenance of biofilms.

In a previous study, the same species behaved similarly when exposed to MPDS in 75 and 100% concentrations under static incubation conditions, simulating the way contact lenses are stored in cases when out of the eyes. There was a moderate reduction in biofilm formation, as well as on P. aeruginosa UFPEDA 416 preformed biofilms. A less encouraging result was found against S. aureus UFPEDA 02. This was possibly due to the difference between biofilm formation rates of the bacteria, with longer delay for P. aeruginosa.[46]

It is noteworthy that the formation of a biofilm is multifactorial and that different strains of the same species may assume different behaviors. A recent study identified the absence of Gram-positive and also the prevalence of MPDS-resistant Gram-negative in the biofilms on contact lens surfaces after 14 days of exposure to a disinfectant solution. This included those contact lenses left in empty wells for the same amount of time. When reconstituted, bacterial regrowth was observed.[37]

Another important point regarding MPDS concerns the nonactivity against some important ocular pathogenic microorganisms, such as Acanthamoeba, whose solutions are more active against trophozoites than cysts. A previous study observed a 1-log unit reduction in the number of cysts to 3-log units of trophozoites.[47] According to the current protocols, the proof of efficacy of an MPDS is considered a reduction of at least 3-log units of planktonic bacterial cells (>99,9%).[48] However, there are no efficiency standards for other microbes as well as for biofilm evaluation, although these structures are more important from a clinical point of view since they are more persistent and therefore represent a higher risk.

Consideration should also be given to microbial multidrug-resistance to different classes of disinfectants and preservatives present in the formulations. Although there is no correlation between a preservative and resistance to antibiotics, some bacteria, especially Gram-negative, may exhibit a multidrug-resistant profile for these two antimicrobial classes and pose serious risks to the wearer's health.[49] In addition, the literature identifies the prevalence of resistance genes to ammonium quaternary compounds.[50] Boric acid was the common compound in the three MPDS. In the available literature, there are no reports of ocular microbiota resistance to this substance. Only one study evaluated the efficacy of 4% boric acid in reducing biofilm formation and concluded that boric acid was less efficient among five antimicrobials tested. Boric acid is considered efficient as an antimicrobial agent to ensure safety; however, it requires high concentrations, which do not represent benefits due to undesirable side effects.[51]

Our hypothesis that ultrasound treatment could potentiate the effect of MPDS resulted in the opposite to the expected. Ultrasound is used to remove aggregated microbial cells on different surfaces and may result in a reduction of 35%–90%. Ultrasound acts by acoustic cavitation, which interacts with the bacteria, resulting in a weakening and disruption of the cell wall, especially in larger cells. The intensity of the ultrasound promotes the formation of bubbles which, when they collapse (cavitation bubbles), produce high-energy shockwaves, with adiabatic gas compression, temperatures around 4500°C, and rotation as a function of torque. The bacteria's sensitivity to sonication is also altered by the aspects of the fluid such as viscosity, sound transfer, and distribution power. Furthermore, when planktonic cells are denser than the surrounding liquid, there is a radiation pressure that can propel them.[52]

40 KHz to  Escherichia More Details coli and Klebsiella pneumoniae may reduce a planktonic cell at 1-log unit after 10 min,[19] revealing that there is a distortion of the concept of the use of ultrasound in the prevention of microbial adhesion on surfaces. This could be confirmed in our study, where the application of low frequency ultrasound resulted the higher susceptibility of S. aureus UFPEDA 02. In addition, when the biofilm was mature the treatment with ultrasound had no effect on either S. aureus or P. aeruginosa UFPEDA 416.

Although ultrasound creates shear forces in the biofilm in the interface with the conditioning substrate, the low frequency is not sufficiently strong enough to disrupt aggregated cells.[53] This is possibly caused by using low frequency (20–100 KHz) and low intensity ultrasound (up to 3 W/cm3) The cell receives only mechanical energy, resulting in a minimum degree of destruction and detachment. Thus, it is postulated that the biocidal effect and cell growth coexist with the use of ultrasound, since these effects depend on the frequency, intensity, material on which ultrasound is applied, as well as the effects of cavitation and presence of viable cells with adherent capacity.[52]

The major propensity for biofilm formation for P. aeruginosa UFPEDA 416 with ultrasound treatment may be the fact that at a low frequency the transport of small nutrient molecules may increase, forming microgradients which favor cell growth. In addition, P. aeruginosa exhibits an extraordinary ability to grow in oligotrophic environment.[54],[55] Moreover, the higher the cell growth rate, the more biofilm will be affected by the ultrasound treatment. P. aeruginosa and S. aureus doubling-times are around 30–40 min.[56] This concept is believed to be able to be applied to different other bacteria with similar doubling-time.[53]

Finally, the high cellular concentration on the CLSC may emphasize two concerns of importance for eye health. The first issue regards the fact that MPDS are effective against planktonic ocular microbial cells, but inhibit their biofilm formation effective. The presence of adherent cells in the medium is a good indication of this problem. The second issue concerns the conduct of good hand hygiene practices, as well as hygiene of the eyelid regions, contact lenses, and their storage cases, including the correct use of disinfectant solutions, essential to reduce the risk of infection. Although new technologies have been searching for more efficient products for the safety and comfort of contact lens wearers, the main risks are still related to hygiene practices as well as overnight use of the lenses.[20] Our results suggest that the patients may not have correctly adhered to good hygiene practices in the handling of contact lenses, a habit that should be encouraged through training and use of efficient evaluation means by ophthalmologists.[57]

   Conclusion Top

Under the experimental conditions, adherent cells of the two most important eye pathogens were detected when exposed to all MPDS under the study. This implied in most cases a moderate to weak inhibition of biofilm formation, as well as results in which no inhibitory effect on adhesion was observed. Among the three brands evaluated, MPDS-C obtained the best results in both in vitro and in vivo assays. Low frequency ultrasound treatment should not be applied as a complementary method for disinfecting the CLSC, especially when the biofilm is already established. Furthermore, good hygiene practices should be taught and promoted among contact lens wearers as well as prospective wearers.

In addition, we recommend vigorous rinsing of contact lenses and their cases, as well as wiping the surfaces on the inside of the case with a clean finger. Friction may facilitate the removal of the formed and structured biofilm, given that immersion in MPDS alone may not guarantee complete elimination of the biofilm. We also endorse the time spam recommended by manufacturers for changing the CLSC may be respected by wearers for their own safety.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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