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Optometry & Vision Science:
doi: 10.1097/OPX.0b013e31821ffccb
Original Article

Influence of Protein Deposition on Bacterial Adhesion to Contact Lenses

Subbaraman, Lakshman N.*; Borazjani, Roya†; Zhu, Hua†; Zhao, Zhenjun†; Jones, Lyndon‡; Willcox, Mark D. P.†

Free Access
Article Outline
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Author Information

*PhD, BSOptom, FAAO

PhD

PhD, FCOptom, FAAO

Brien Holden Vision Institute, Sydney, New South Wales, Australia (LNS, HZ, ZZ, MDPW), Alcon Research Ltd, Fort Worth, Texas (RB), Centre for Contact Lens Research, School of Optometry, University of Waterloo, Waterloo, Ontario, Canada (LJ), and School of Optometry and Vision Science, University of New South Wales, Sydney, New South Wales, Australia (MDPW).

LNS was a recipient of the American Optometric Foundation's William C. Ezell Fellowship.

This work was presented in part as podium presentations at the American Academy of Optometry Annual Meeting 2008, Anaheim, CA, British Contact Lens Association Conference 2009, Birmingham, UK, and the 15th International Society for Contact Lens Research Symposium 2009, Crete, Greece.

Received October 28, 2010; accepted April 4, 2011.

Lakshman N. Subbaraman; Department of Chemical Engineering; McMaster University; 1280 Main Street West; Hamilton, Ontario, Canada L8S 4L7; e-mail: slaksh@mcmaster.ca

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Abstract

Purpose. The aim of the study is to determine the adhesion of Gram positive and Gram negative bacteria onto conventional hydrogel (CH) and silicone hydrogel (SH) contact lens materials with and without lysozyme, lactoferrin, and albumin coating.

Methods. Four lens types (three SH—balafilcon A, lotrafilcon B, and senofilcon A; one CH—etafilcon A) were coated with lysozyme, lactoferrin, or albumin (uncoated lenses acted as controls) and then incubated in Staphylococcus aureus (Saur 31) or either of two strains of Pseudomonas aeruginosa (Paer 6294 and 6206) for 24 h at 37°C. The total counts of the adhered bacteria were determined using the 3H-thymidine method and viable counts by counting the number of colony-forming units on agar media.

Results. All three strains adhered significantly lower to uncoated etafilcon A lenses compared with uncoated SH lenses (p < 0.05). Lysozyme coating on all four lens types increased binding (total and viable counts) of Saur 31 (p < 0.05). However, lysozyme coating did not influence P. aeruginosa adhesion (p > 0.05). Lactoferrin coating on lenses increased binding (total and viable counts) of Saur 31 (p < 0.05). Lactoferrin-coated lenses showed significantly higher total counts (p < 0.05) but significantly lower viable counts (p < 0.05) of adhered P. aeruginosa strains. There was a significant difference between the total and viable counts (p < 0.05) that were bound to lactoferrin-coated lenses. Albumin coating of lenses increased binding (total and viable counts) of all three strains (p < 0.05).

Conclusions. Lysozyme deposited on contact lenses does not possess antibacterial activity against certain bacterial strains, whereas lactoferrin possess an antibacterial effect against strains of P. aeruginosa.

Bacterial colonization of contact lenses is one of the initiating factors in many adverse responses that occur during contact lens wear.1,2 Bacterial adhesion to the contact lens material is the first step in a series of events that leads to contact lens-related infection or inflammation.2,3

The tear film is composed of several proteins including lysozyme, lactoferrin, and immunoglobulin A, which have an antibacterial and/or bacteriostatic role.4–6 In addition, mechanical defenses such as blinking and tear flow assist the eye in eliminating bacteria from the ocular surface.4 During contact lens wear, a protein-rich coating, or conditioning film, forms on the contact lens surface.7–10 It has recently been shown that more than 60 proteins are deposited onto contact lens materials and some of the major sorbed tear film components include lysozyme, lactoferrin, and albumin.11,12

Most previous studies have determined the influence of deposits on bacterial adhesion only on conventional polyHEMA-based hydrogel contact lens materials13–23; however, to date, no study has investigated the influence of deposits on bacterial adhesion to silicone hydrogel (SH) contact lens materials. Albumin coated onto the surface of etafilcon A or polymacon contact lenses increased the adhesion of Pseudomonas aeruginosa.18 Similarly, some strains of Serratia marcescens adhered more to etafilcon A lenses coated in an artificial tear fluid.24 Lysozyme adsorbed to etafilcon A contact lenses has been reported to increase or to not modulate the adhesion of Staphylococcus aureus.16,25 Lactoferrin deposited on the surface of etafilcon A lenses promotes the adhesion of P. aeruginosa strain Paer 1; nevertheless, once adherent, this protein reduces the proportion of viable bacteria on the lens surface.17 To date, few studies have investigated the adhesion of bacteria to SH lens materials, and none of these studies have determined the influence of tear components on the adhesion of bacteria to such materials.

Thus, the purpose of this study was to examine the effect of the contact lens conditioning film on bacterial adhesion by comparing the adhesion of three different bacterial strains to uncoated contact lenses and to contact lenses that were coated with individual major tear proteins (lysozyme, lactoferrin, and albumin). The other purpose of the study was to determine whether the presence of these individual tear proteins had any effect on the viability of the attached bacteria.

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MATERIALS AND METHODS

Contact Lenses

The SH lens materials examined in this study were lotrafilcon B (Air Optix; CIBA Vision, Duluth, GA), balafilcon A (PureVision; Bausch & Lomb, Rochester, NY), and senofilcon A (Acuvue OASYS; Vistakon, Johnson & Johnson, Jacksonville, FL). The conventional hydrogel (CH) lens material examined was etafilcon A (Acuvue 2; Vistakon, Johnson & Johnson). The properties of these lens materials are described in Table 1.

Table 1
Table 1
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Treatment of Uncoated Lens Materials

Three test and control lenses from each lens type were used for adhesion assays for each strain, and each experiment was repeated at least twice. Contact lenses were removed from their packaging and thoroughly rinsed in sterile phosphate buffered saline (PBS), pH 7.4, for 1 h to ensure that no packaging solution remained on the lens surface. These lenses were considered “uncoated lenses” and acted as controls.

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Protein Coating on Contact Lenses

Lenses of each lens type were coated with three different tear proteins: lysozyme, lactoferrin, and albumin (Sigma-Aldrich, Castle Hill, NSW, Australia). Lysozyme, lactoferrin, and albumin solutions were prepared at a concentration of 1.9, 1.9, and 0.5 mg/ml respectively. The lenses were incubated at the specified concentration for the following time period based on the results from previously published studies.26–28 The CH lens material was incubated in the lysozyme solution for 5 days, while the SH lens materials were incubated for 7 days. All the lenses were incubated in lactoferrin and albumin solutions for 7 days. After the specified incubation periods, the lenses were removed from the vials and washed in a plate shaker with PBS to remove loosely bound protein. These lenses were the “protein-coated” lenses.

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Bacterial Preparation

Three bacterial strains were investigated in this study, of which one was a Gram positive strain (S. aureus 31; Saur 31) and two were Gram negative strains (P. aeruginosa 6206 and 6294; Paer 6206 and 6294). The Gram positive Saur 31 was isolated from a patient with contact lens-induced peripheral ulcer. Both strains of Paer used in this study (6294 and 6206) were isolated from human microbial keratitis specimens, and strain 6206 has been shown to be a cytotoxic strain, whereas strain 6294 is an invasive strain.29

Stock cultures of Saur 31, Paer 6206, and Paer 6294 were stored in 30% glycerol at −80°C. Bacteria were grown overnight in 10 ml of Tryptone Soy Broth (TSB; Oxoid, Sydney, Australia) at 37°C for 18 h. Bacterial cells were harvested by centrifugation (Eppendorf 5810, Eppendorf AG, Hamburg, Germany) for 10 min (3000 rpm at 18°C) and washed in sterile PBS. The bacterial cells were then resuspended in sterile PBS, and the concentration was adjusted using a spectrophotometer (Helios β, Unicam Instruments, Cambridge, UK) to give an optical density of 0.1 at 660 nm, which gave 1.0 × 108 colony-forming units (CFU)/ml.

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Determination of Viable Counts of Bacteria on Lenses

The uncoated and protein-coated lenses were then placed in a 24-well plate containing 1 ml of bacterial suspension and incubated at 37°C for 24 h with PBS as the medium. After 24 h, the lenses were removed and shaken for 30 s on a plate shaker at 175 rpm to remove loosely adherent bacteria. The lenses were then washed three times in 1 ml of sterile PBS for 30 s each time, transferred to a sterile 5 ml plastic container (Greiner Bio-One, Longwood, FL), and vortexed vigorously for 1 min in 2 ml of sterile PBS, using sterile magnetic stirring bars. Pilot studies demonstrated that the vortex procedure homogenized the lenses and resulted in >99.9% of bacteria being removed from the lenses. For quantitation of viable bacteria per contact lens, the homogenate was serially diluted in PBS 1:10 by taking 100 μl and adding it to 900 μl of neutralizing broth (Difco Laboratories, Detroit, MI) in a microcentrifuge tube. Fifty microliters of the serially diluted samples were plated in triplicate on nutrient agar plates (Oxoid, Sydney, Australia) and incubated for 18 h at 37°C. Dilutions with growth between 10 and 100 colonies were counted on a colony counter. The number of colonies per dilution were recorded and used to calculate the number of CFU per contact lens. Each assay used three lenses of each type and was repeated twice, and then the average values were computed to enumerate the viable counts of the bacteria adhered to contact lenses.

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Determination of Total Counts of Bacteria on Lenses

Stock cultures of Saur 31, Paer 6206, and Paer 6294 were grown in 10 ml of Tryptone Soy Broth (TSB; Oxoid, Sydney, Australia) and 3H-thymidine (80 μCi) for 18 h. Bacterial cells were harvested by centrifugation (Eppendorf 5810, Eppendorf AG, Hamburg, Germany) for 15 min (3000 rpm at 18°C) and washed in sterile PBS three times. The bacterial cells were then resuspended in sterile PBS and 1 μCi/ml of 3H-thymidine and the concentration was adjusted using a spectrophotometer (Helios β, Unicam Instruments, Cambridge, UK) to give an optical density of 0.1 at 660 nm. The protein-coated and uncoated lenses were then placed in a 24-well plate containing 1 ml of radiolabeled bacterial suspension in each well and incubated at 37°C for 24 h. After 24 h of incubation, the lenses were removed from the incubator and shaken for 30 s on a plate shaker at 175 rpm to remove loosely adherent bacteria. The lenses were then washed three times in 1 ml of sterile PBS for 30 s. The vials were then placed with 500 μl 0.2M NaOH at 80°C for 1 h, following which they were allowed to cool down by placing them on ice. Scintillation fluid was then added to the vials and the counts per minute were determined using a Beta counter. A standard curve was plotted to determine the CFU/lens values of total counts of adhered bacteria.

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Statistical Analysis

Statistical analysis was conducted using Statistica 7 software (StatSoft, Tulsa, OK). All data are reported as mean ± SD. A factorial analysis of variance was performed with lens type, protein coating, and viability as the factors. Post hoc multiple comparison testing was undertaken using the Tukey's HSD test. In all cases, a p value <0.05 was considered significant.

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RESULTS

Bacterial Adhesion to Uncoated Lens Materials

Among the SHs, the adhesion was highest on balafilcon A and lotrafilcon B lens materials, when compared with the senofilcon A material (p < 0.05). There was no significant difference between the total and viable counts (p > 0.05) of all the three strains that were bound to uncoated lenses. All three tested strains adhered at a significantly lower level to uncoated etafilcon A lenses when compared with uncoated SH lens materials (p < 0.05; Fig. 1).

Figure 1
Figure 1
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Effect of Lysozyme Coating on Bacterial Adhesion

Fig. 2a shows the adhesion of Gram positive Saur 31 to uncoated and lysozyme-coated contact lens materials. There was no significant difference between the viable and total counts for lysozyme-coated lenses (p > 0.05 for all lens types). When compared with uncoated lenses, there was a significant increase in the viable and total counts of Saur 31 adhered to the lysozyme-coated lenses for all lens types (p < 0.05 for all lens types). Among the lysozyme-coated lens materials, there was no significant difference in Saur 31 adhesion between balafilcon A and lotrafilcon B (p > 0.05) and no significant difference in Saur 31 adhesion between senofilcon A and etafilcon A lens materials (p > 0.05). Lysozyme-coated senofilcon A and etafilcon A lens materials showed significantly lower Saur 31 binding than lysozyme-coated balafilcon A and lotrafilcon B lens materials (p < 0.05).

Figure 2
Figure 2
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Fig. 2b, c shows the adhesion of Gram negative Paer 6206 and 6294 strains to uncoated and lysozyme-coated contact lens materials. There was no significant difference between the viable and total counts for lysozyme-coated lenses (p > 0.05 for all lens types). When compared with uncoated lenses, there was no significant increase in the viable and total counts of Paer 6206 and 6294 strains adhered to lysozyme-coated lenses for all lens types (p > 0.05 for all lens types). Among the lysozyme-coated lens materials, there was no significant difference in Paer 6206 and 6294 adhesion between balafilcon A and lotrafilcon B (p > 0.05), and etafilcon A lenses showed the lowest (p < 0.05) adhesion of Paer 6206 and 6294 strains. Binding of Paer strains to lysozyme-coated senofilcon A was significantly lower than lysozyme-coated balafilcon A and lotrafilcon B lenses (p < 0.05) but higher than etafilcon A lenses (p < 0.05).

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Effect of Lactoferrin Coating on Bacterial Adhesion

Fig. 3a shows the adhesion of Gram positive Saur 31 to uncoated and lactoferrin-coated contact lens materials. There was no significant difference between the viable and total counts for lactoferrin-coated lenses (p > 0.05 for all lens types). When compared with uncoated lenses, there was a significant increase in the viable and total counts of Saur 31 adhered to the lactoferrin-coated lenses for all lens types (p < 0.05 for all lens types). Among the lactoferrin-coated lens materials, there was no significant difference in Saur 31 adhesion between balafilcon A and lotrafilcon B (p > 0.05), and lactoferrin-coated etafilcon A lens material showed the least adhesion of Saur 31 (p < 0.05). Binding of Saur 31 to lactoferrin-coated senofilcon A was significantly lower than lactoferrin-coated balafilcon A and lotrafilcon B lenses (p < 0.05) but higher than etafilcon A lenses (p < 0.05).

Figure 3
Figure 3
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Fig. 3b, c shows the adhesion of Gram negative Paer 6206 and 6294 strains to uncoated and lactoferrin-coated contact lens materials. There was a significant difference between the total and viable counts (p < 0.05) bound to lactoferrin-coated lenses. When compared with uncoated lenses, all four lactoferrin-coated lens types showed significantly higher total counts (p < 0.05) of adhered Paer strains, whereas the lactoferrin-coated lenses showed significantly lower viable counts (p < 0.05) of adhered Paer strains.

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Effect of Albumin Coating on Bacterial Adhesion

Fig. 4a shows the adhesion of Gram positive Saur 31 to uncoated and albumin-coated contact lens materials. There was no significant difference between the viable and total counts for albumin-coated lenses (p > 0.05 for all lens types). When compared with uncoated lenses, there was a significant increase in the viable and total counts of Saur 31 adhered to the albumin-coated lenses for all lens types (p < 0.05 for all lens types). Among the albumin-coated lens materials, there was no significant difference in Saur 31 adhesion between balafilcon A and lotrafilcon B (p > 0.05) and no significant difference in Saur 31 adhesion between senofilcon A and etafilcon A lenses (p > 0.05). Albumin-coated senofilcon A and etafilcon A lenses showed significantly lower Saur 31 binding than albumin-coated balafilcon A and lotrafilcon B lenses (p < 0.05).

Figure 4
Figure 4
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Fig. 4b, c show the adhesion of Gram negative Paer 6206 and 6294 strains to uncoated and albumin-coated contact lens materials. There was no significant difference between the viable and total counts for albumin-coated lenses (p > 0.05 for all lens types). When compared with uncoated lenses, there was a significant increase in the viable and total counts of Paer 6206 and 6294 strains adhered to albumin-coated lenses for all lens types (p < 0.05 for all lens types). Among the albumin-coated lens materials, there was no significant difference in Paer 6206 and 6294 adhesion between balafilcon A and lotrafilcon B (p > 0.05) and no significant difference in the adhesion of Paer 6206 and 6294 strains between the albumin-coated senofilcon A and etafilcon A lenses (p > 0.05). Albumin-coated senofilcon A and etafilcon A lenses showed significantly lower binding of Paer 6206 and 6294 strains than albumin-coated balafilcon A and lotrafilcon B lenses (p < 0.05).

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DISCUSSION

This is the first study to determine the effect of individual tear proteins on bacterial adhesion to SH contact lens materials. These results demonstrate that different tear proteins deposited on contact lenses have varying effects on the adhesion of bacteria to contact lenses. Historically, there has been disagreement concerning the effects of protein conditioning on the adhesion of bacteria to hydrogel contact lenses. Initial studies showed that bacteria readily adhered to unworn contact lenses,30 but adhesion was shown to increase in patient-worn lenses.13,15,21,31 Conversely, other studies showed that there was no increase20,32 or inhibition of bacterial adhesion to patient-worn lenses23 when compared with unworn lenses.

Miller and Ahearn33 reported that mucin, immunoglobulin A, bovine serum albumin, lysozyme, and lactoferrin coated onto unworn lenses enhanced the adhesion of P. aeruginosa to hydrogel contact lens materials. Williams et al.17 showed that lactoferrin coated onto the surface of etafilcon A promoted the adhesion of P. aeruginosa strain Paer 1; nevertheless, once adherent, this protein reduced the proportion of viable bacteria on the lens surface. A similar finding was demonstrated in the current study for lactoferrin adsorbed to etafilcon A lenses and three SH lenses. To our knowledge, this is the first study that has shown that lactoferrin bound to SH lenses have an antibacterial effect against P. aeruginosa strains. Lactoferrin has traditionally been regarded as a bacteriostatic protein, because it sequesters the iron that bacteria require for growth.34 However, lactoferrin possesses direct bactericidal effects.35,36 Lactoferrin destabilizes the lipopolysaccharide (LPS) of Gram negative bacteria by targeting either the metal cations that stabilize the negative charge of the LPS37,38 or the LPS directly.35,39 Therefore, lactoferrin may exert its bactericidal effect after adsorption to a contact lens surface by destabilizing the outer membrane (LPS) of the Gram negative bacteria P. aeruginosa. We have previously determined that lactoferrin at a concentration of 2 mg/ml in a defined salts medium allows P. aeruginosa to grow,40 suggesting that lactoferrin in PBS does not have a bactericidal effect. The results from this study clearly show that lactoferrin bound to contact lenses has an antibacterial effect and further work is needed to determine the exact mechanism behind this.

Albumin coated onto the surface of etafilcon A or polymacon contact lenses increased the adhesion of P. aeruginosa.18 The results from the previous study demonstrated that Staphylococcus epidermidis and P. aeruginosa adhered significantly higher with increasing concentration of albumin on contact lenses.18 The results from this study are in accordance with the previous studies and the results from the current study also suggest that albumin-coating on contact lenses do not possess an antibacterial effect against the three bacterial strains tested in this study.

Thakur et al.16 demonstrated that lysozyme adsorbed to a contact lens increased the adhesion of S. aureus to etafilcon A contact lenses. In contrast, Zhang et al.25 demonstrated that lysozyme adsorbed to etafilcon A and balafilcon A lenses did not affect the adhesion (viable or total) of S. aureus or P. aeruginosa strains, and this agrees with results from the current study with other SH lenses for Paer strains. The bactericidal effects of lysozyme are most potent against Gram positive bacteria which, unlike Gram negative bacteria, lack an extra outer membrane around the peptidoglycan layer targeted by lysozyme.41,42 Surprisingly, the results from this study show that lysozyme deposited on the lens materials does not possess an antibacterial effect against either the Gram positive or Gram negative strains tested in this study. It is known that once lysozyme deposits on conventional and SH contact lens material, it tends to undergo conformational changes,9,43–48 which could potentially result in the loss of antibacterial activity against these strains of bacteria.

The results from the current study suggest that there was an increased binding of all three strains of bacteria to the tested uncoated SH lens materials, when compared with one type of uncoated CH lens material. Among the SHs, the adhesion was highest on balafilcon A and lotrafilcon B lens materials, when compared with the senofilcon A material. Bacterial adhesion to a biomaterial is known to depend on the hydrophobicity or hydrophilicity of the biomaterial and therefore on the nature of the polymer of the contact lens.19,49–53 Furthermore, the water content of the lens material is also known to affect the adhesion of bacteria, decreasing with increasing water content of the lens material.51,54,55 The results from this study agree with these findings, in that etafilcon A, the material with the highest water content (58%) of the four contact lenses, demonstrated the lowest bacterial binding, whereas the opposite was true for the lotrafilcon B material. These results are in accordance with other published studies that have compared the bacterial adhesion to conventional and SH contact lens materials.51–53 This study has demonstrated that bacteria generally bind in higher levels to SH contact lenses. As bacterial adhesion to lenses may be the first step in a series of events that leads to several contact lens-related adverse events, this increase in adhesion may be one of the factors in the increased rates of corneal infiltrative events that have been reported with SH lenses.56

Further investigation is required to determine the adhesion of more bacterial strains that are involved in the pathogenesis of contact lens-related infections. Furthermore, it will be of significant clinical relevance to evaluate the impact of various care regimens and the impact of “rub and rinse” steps on bacterial adhesion to contact lenses. This study has demonstrated that lactoferrin coating on contact lenses has the ability to reduce the viability of P. aeruginosa strain and that it may be worthwhile to develop antibacterial contact lenses with some form of lactoferrin coating, which might potentially reduce the risk of corneal infection.

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ACKNOWLEDGMENTS

This work was supported by Natural Sciences and Engineering Research Council of Canada and Alcon Research Limited, Fort Worth, Texas.

Lakshman N. Subbaraman

Department of Chemical Engineering

McMaster University

1280 Main Street West

Hamilton, Ontario, Canada L8S 4L7

e-mail: slaksh@mcmaster.ca

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Impact of tear film components on the conformational state of lysozyme deposited on contact lenses
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10.1002/jbm.b.32927
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Keywords:

bacterial attachment; contact lens; protein deposition; Pseudomonas; silicone hydrogel; Staphylococcus

© 2011 American Academy of Optometry

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