Combining the adhesion data for all three Pseudomonas strains (Table 3; Fig. 1B), significant differences in levels of bacterial adhesion were observed among test lens types. The differences were as follows: (1) total adhesion to unworn lotrafilcon B, enfilcon A, comfilcon A, filcon II 3, or lotrafilcon A was greater than to unworn narafilcon A (p ≤ 0.002), galyfilcon A (p ≤ 0.021), senofilcon A (p ≤ 0.008), or asmofilcon A (p ≤ 0.004); (2) total adhesion to unworn balafilcon A was significantly less than to unworn lotrafilcon B (p = 0.037), comfilcon A (p = 0.000), or lotrafilcon A (p = 0.007); (3) viable adhesion to unworn asmofilcon A was significantly less than to all other lens types (p ≤ 0.001) except unworn narafilcon A (p = 0.468) or balafilcon A (p = 1.000); (4) viable adhesion to unworn balafilcon A was significantly less than to all other lens types (p = 0.000) except unworn narafilcon A (p = 0.267) or asmofilcon A (p = 1.000); (5) viable adhesion to unworn narafilcon A was significantly less than to unworn comfilcon A (p = 0.000) or filcon II 3 (p = 0.001) only.
Comparing P. aeruginosa strains, total counts of P. aeruginosa 6206 were significantly higher than P. aeruginosa 6294 (Table 4). Overall, there was no significant difference between the strains for viable counts on unworn lenses (Table 4). Regardless of the lens polymer type, P. aeruginosa strains adhered in greater numbers to unworn lenses compared with S. aureus strains (p < 0.001).
Adhesion to Worn Lenses
Table 3 and Fig. 1C, D show the mean adhesion of the combined strains with 95% confidence intervals.
Combining the adhesion data for all three Staphylococcus strains (Table 3; Fig. 1C), significant differences in levels of bacterial adhesion were observed among test lens types. The differences were as follows: (1) total adhesion to worn asmofilcon A was significantly less (p ≤ 0.01) than to all other worn lenses except to worn galyfilcon A (p = 1.000) and worn balafilcon A (p = 0.665); (2) total adhesion to worn filcon II 3 was significantly greater (p ≤ 0.028) than to all other worn lenses except to narafilcon A (p = 0.893) and lotrafilcon A (p = 0.475); (3) total adhesion to worn narafilcon A was significantly greater than to worn galyfilcon A (p = 0.000), asmofilcon A (p = 0.000), or balafilcon A (p = 0.021); (4) total adhesion to worn lotrafilcon A was significantly greater than to worn galyfilcon A (p = 0.004) or asmofilcon A (p = 0.000) or balafilcon A (p = 0.029); (5) viable adhesion to worn asmofilcon A was significantly less (p = 0.000) than to all other worn lenses except to worn filcon II 3 (p = 1.000) and worn balafilcon A (p = 0.751); (6) viable adhesion to worn balafilcon A was significantly less than to worn narafilcon A (p = 0.002), worn senofilcon A (p = 0.000), and worn lotrafilcon A (p = 0.029); (7) viable adhesion to worn lotrafilcon A was significantly greater than to worn filcon II 3 (p = 0.021), worn asmofilcon A (p = 0.000), and worn balafilcon A (p = 0.029); (8) viable adhesion to worn filcon II 3 was significantly less than to worn narafilcon A (p = 0.001), worn senofilcon A (p = 0.000), and worn lotrafilcon A (p = 0.021); (9) viable adhesion to worn enfilcon A was significantly less than to worn senofilcon A (p = 0.024).
For the individual S. aureus strains, the order of viable adhesion on worn lenses was S. aureus 31 > S. aureus ATCC 6538 (p = 0.000) > S. aureus 38 (p = 0.000; Table 3). S. aureus 38 adhered least to worn lenses (regardless of lens type; Table 4).
Combining the adhesion data for all three Pseudomonas strains (Table 3; Fig. 1D), significant differences in levels of bacterial adhesion were observed among test lens types. The differences were as follows: (1) total adhesion to worn asmofilcon A was significantly lower than to worn narafilcon A (p = 0.000), worn enfilcon A (p = 0.000), worn comfilcon A (p = 0.023), and worn filcon II 3 (p = 0.004); (2) total adhesion to worn enfilcon A was significantly higher than to worn galyfilcon A (p = 0.000), worn senofilcon A (p = 0.001), worn lotrafilcon B (p = 0.000), and worn asmofilcon A (p = 0.000); (3) total adhesion to worn galyfilcon A was significantly lower than to worn narafilcon A (p = 0.006) or enfilcon A (p = 0.000); (4) viable adhesion to worn narafilcon A was significantly (p ≤ 0.001) higher than to all other lenses except worn enfilcon A (1.000), worn comfilcon A (0.483), or worn filcon II 3 (0.170); (5) viable adhesion to worn enfilcon A was significantly (p ≤ 0.006) higher than to all other lenses except for worn narafilcon A (p = 1.000), worn comfilcon A (p = 1.000) or worn filcon II 3 (p = 0.596); (6) viable adhesion to worn asmofilcon A was significantly less than to worn narafilcon A (p = 0.000), worn enfilcon A (p = 0.000), worn comfilcon A (p = 0.001), and worn filcon II 3 (p = 0.001); (7) viable adhesion to worn galyfilcon A was significantly less than to worn narafilcon A (p = 0.000), worn enfilcon A (p = 0.000), or worn comfilcon A (p = 0.031).
Combining adhesion data from all the worn lens materials (Table 4), P. aeruginosa 6206 showed the least viable counts compared with the other strains, whereas strain GSU-3 showed the least total counts compared with strain 6206 only (p < 0.05). Similar to the unworn lenses, P. aeruginosa strains adhered in greater numbers to all silicone hydrogel lens materials compared with S. aureus strains.
Effect of Lens Wear on Adhesion
There were more total than viable S. aureus adherent to all the lens materials after wear (Table 3; Fig. 1C). For S. aureus overall, significantly higher numbers of total bacterial cells adhered to worn narafilcon A, enfilcon A, and filcon II 3 lenses compared with the unworn lenses (p < 0.05). No significant differences were observed for the overall number of viable cells on worn compared with unworn lenses.
S. aureus 31 showed significantly higher total adhesion to worn compared with unworn narafilcon A, senofilcon A, lotrafilcon B, enfilcon A, comfilcon A, and asmofilcon A lenses (p ≤ 0.009, Fig. 2). The viable adhesion of S. aureus 31 on most of the worn lenses was similar to unworn lenses except for increases in adhesion to senofilcon A (p = 0.003) and enfilcon A (p = 0.000) lenses. S. aureus 38 showed significantly less total adhesion to worn compared with unworn senofilcon A and balafilcon A lenses (p ≤ 0.03, Fig. 2); no significant differences were seen for the other lens materials. S. aureus 38 had higher levels of viable cells adhered to worn narafilcon A, enfilcon A, and comfilcon A lenses compared with unworn lenses (p ≤ 0.041, Fig. 2). Total adhesion of S. aureus ATCC 6538 was not affected by wear to any lens type. Lens wear reduced the numbers of viable S. aureus ATCC 6538 on galyfilcon A, lotrafilcon B, and lotrafilcon A, but increased the numbers of viable cells on asmofilcon A lenses compared with unworn lenses (p ≤ 0.015, Fig. 2).
When the effect of lens wear on overall adhesion of P. aeruginosa was analyzed using combined data from three test strains, there was a significant increase in Pseudomonas total adhesion to narafilcon A lenses (p = 0.0001) compared with unworn lenses, whereas significantly lower total numbers adhered to worn comfilcon A lenses (p < 0.05) compared with unworn lenses. Lower viable numbers of P. aeruginosa adhered to worn galyfilcon A, lotrafilcon B, and lotrafilcon A lenses (p < 0.05) compared with unworn lenses, but higher viable numbers adhered to worn balafilcon A lenses (p < 0.05) compared with unworn lenses.
Significantly lower numbers of viable P. aeruginosa 6206 adhered to worn galyfilcon A (p = 0.042) compared with unworn lenses. Significantly higher total adhesion of P. aeruginosa 6294 was seen to worn senofilcon A lenses (p = 0.024, Fig. 2) compared with unworn lenses. Significantly higher numbers of viable cells of P. aeruginosa 6294 adhered to worn narafilcon A (p = 0.003) or enfilcon A (p = 0.042) lenses compared with unworn lenses. P. aeruginosa GSU-3 showed significantly higher total adhesion to worn narafilcon A lenses (p = 0.003, Fig. 2) compared with unworn lenses, but there was significantly lower total adhesion of cells to worn lotrafilcon B (p = 0.001) or comfilcon A (p = 0.005) lenses compared with unworn lenses. There was significantly increased adhesion of viable GSU-3 to worn narafilcon A lenses (p = 0.000), but lower numbers of viable cells adhered to worn lotrafilcon B (p = 0.000) or comfilcon A (p = 0.008) lenses compared with unworn lenses.
Correlations between Bacterial Adhesion and Contact Lens Polymer and Surface Properties
Correlations were sought for data on the contact lens properties (Table 2) and bacterial adhesion (Table 3). There was a relatively strong (r > ±0.5) correlation between lens oxygen permeability and adhesion for S. aureus total cells; the higher the oxygen permeability, the higher the adhesion (Table 5). However, overall, there was no strong relationship between bacterial adhesion and oxygen permeability of a lens, as this was the only correlation seen for this material property. There was a relatively strong correlation (r > −0.5) between adhesion of S. aureus (total or viable cells) and the water content of a lens such that the higher the water content of the lens, the lower the adhesion of S. aureus.
In general, there were moderate (±0.3 ≤ r ≤ ±0.5) to strong (r > ±0.5) correlations between Pseudomonas or Staphylococcus adhesion and contact lens surface hydrophobicity (however measured) such that the more hydrophobic the surface, the less bacterial adhesion there was. In particular, there was a strong correlation between total adhesion of P. aeruginosa and contact angle measured by receding captive bubble, advancing sessile drop, or Wilhelmy balance techniques (Table 5); a strong correlation between viable adhesion of P. aeruginosa and contact angle measured by advancing captive bubble, advancing sessile drop, or Wilhelmy balance techniques (Table 5); and a strong correlation between total adhesion of S. aureus and advancing captive bubble, advancing sessile drop, or Wilhelmy balance techniques (Table 5).
The number of total or viable P. aeruginosa that adhered to lenses appeared to be dependent on the surface roughness and surface energy of the contact lenses such that surfaces with higher roughness or lower surface energy tended to adhere fewer bacterial cells (Table 5). There was no such relationship to total or viable S. aureus adhesion.
This study found that strains of P. aeruginosa adhere in higher numbers than strains of S. aureus to silicone hydrogel lenses, regardless of lens polymer type or surface properties of the lens. For both bacterial genera, there was a relationship between the surface hydrophobicity of the lens and numbers of bacterial cells adhering to the lens. Wearing the contact lenses for 1 day (on a daily disposable basis) had different effects on adhesion of the bacteria, depending on the bacterial strain and lens type. Bacterial adhesion to contact lenses may be significant, as it is likely to be the initial event in the production of adverse responses, such as MK, contact lens-induced acute red eye, and contact lens-induced peripheral ulcers.
The finding that P. aeruginosa strains tend to adhere to contact lenses in higher numbers than other bacterial types has been previously reported by others. Kodjikian et al.25 found that the number of viable P. aeruginosa cells on lenses was generally higher than the number of viable Staphylococcus epidermidis. Henriques et al.24 also found that a strain of S. epidermidis (strain 12,228) adhered in lower numbers to lotrafilcon A and balafilcon A (as well as the HEMA-based etafilcon A) lenses than a strain of P. aeruginosa (10145). However, another strain of S. epidermidis (9142) adhered to these silicone hydrogel lens types in similar numbers as the strain of P. aeruginosa. P. aeruginosa strains 6206 and 6294 previously have been shown to adhere in higher numbers to unworn etafilcon A, lotrafilcon A,39 senofilcon A, or balafilcon A39,40 lenses compared with S. aureus strain 31, and this was confirmed in the present study. Using one of the same strains as in the current study, namely, P. aeruginosa GSU-3 (strain 328), Bruinsma et al.28 found that P. aeruginosa GSU-3, with a relatively hydrophobic cell surface, adhered in higher numbers to contact lenses (type of contact lens not stated) than the relatively hydrophilic S. aureus 799, and this was regardless of whether the lenses had been soaked in tears. The ability of P. aeruginosa to adhere in high numbers to many contact lens types may be one of the reasons that this bacterium is the predominant causative microbe for contact-lens–related MK,9,11,19–21 and it can also cause other adverse events.14,29
Using a method (ATP bioluminescence) that measures numbers of viable bacteria adhered to a surface, Kodjikian et al.25 found that two strains of S. epidermidis and one strain of P. aeruginosa adhered maximally to unworn lotrafilcon B lenses, and one strain of S. epidermidis and the strain of P. aeruginosa adhered better to unworn balafilcon A lenses than unworn galyfilcon A lenses. The lotrafilcon B lenses used in the Kodjikian et al.25 study were slightly different than those used in the current assay, as they were an older version that did not contain the “AQUA” internal wetting agent. Even so, in the current study, the number of viable cells of P. aeruginosa or S. aureus was generally greater on unworn lotrafilcon B lenses than on unworn galyfilcon A or balafilcon A lenses.
The effect of the hydrophobicity of substrata on bacterial adhesion is somewhat controversial. Fletcher and Loeb41 showed that adhesion of a marine pseudomonad was driven by surface hydrophobicity such that advancing contact angles and bacterial adhesion had a correlation coefficient of 0.73 (R2 = 0.54), i.e., the more hydrophobic the substratum, the higher the adhesion. Similarly, Fletcher and Marshall42 found that more hydrophobic surfaces tend to adhere more of a particular strain of Pseudomonas. Giraldez et al.37 found that, when comparing adhesion of S. epidermidis with three HEMA-based and two silicone hydrogel contact lenses, the hydrophobicity of the lens surface was partly correlated to adhesion; the more hydrophobic silicone hydrogel lenses adhere more viable bacterial cells than the less hydrophobic HEMA-based lenses. However, the formation of dental plaque on surfaces in the human oral cavity is far less on hydrophobic than on hydrophilic surfaces.43 Hydrophobic silicone rubber voice prostheses in patients who had had a laryngectomy were contaminated by less biofilm than a prosthesis with a relatively hydrophilic surface.44 Tang et al.,45 using silicone samples but not contact lenses, showed that adhesion of S. epidermidis (measured by counting viable cells) decreased with increasing substrate hydrophobicity. Data from the present study suggest that adhesion of P. aeruginosa or S. aureus is generally less to more hydrophobic silicone hydrogel lenses. Henriques et al.24 reported the advancing contact angle of balafilcon A, lotrafilcon A, and galyfilcon A lenses after they had been soaked in artificial tear fluid to be approximately 75°, 51°, and 35°. If these values are substituted for the values of non–artificial tear-soaked lenses and then compared with adhesion of P. aeruginosa or S. aureus to these lens types after wear from the present study, the correlation coefficients (r) for P. aeruginosa are 0.75 and 0.85 for total and viable cells, respectively, and for S. aureus, they are 0.07 and −0.99 for total and viable cells, respectively. In general, the contact angles are reduced after soaking in artificial tear fluid (especially for galyfilcon A), and this leads to (at least for P. aeruginosa) a change in adhesion characteristics such that adhesion (total or viable) is now increased with increasing hydrophobicity. This result from the current investigation is in general agreement with Henriques et al.24 and their reported adhesion data. Bruinsma et al.28 also found that adsorbing tears to contact lenses (types not stated) generally decreased their surface hydrophobicity. The current study did not examine the adhesion to any conventional HEMA-based hydrogel materials. However, Kodjikian et al.25 found that a strain of P. aeruginosa adhered to a HEMA-based (etalfilcon A) or silicone hydrogel lenses in higher numbers than two strains of S. aureus. If the data from Kodjikian et al.25 are compared with the data from Read et al.,31 who examined the surface contact angle using the advancing sessile drop technique for the same HEMA-based and silicone hydrogel lenses, it appears that adhesion to the HEMA-based lenses is less for both genera of bacteria, and that the relationship between adhesion and surface hydrophobicity is parabolic [equation for P. aeruginosa is adhesion = −0.02(contact angle)2 + 2.6775 × –22.535; R2 = 0.92; for S. aureus is adhesion = y = −0.0006(contact angle)2 + 0.0759 × –0.3005; R2 = 0.6294] with a maximum adhesion lying between 40° and 60° for both genera, and a rapid decline toward minima below 20° or at or above 100°.
When adhesion to surfaces with similar hydrophobicities, but differing surface roughness, was examined, a higher surface roughness resulted in an increase in bacterial adhesion.45 The present study found that surface roughness was moderately to strongly negatively correlated with adhesion of total or viable P. aeruginosa, but not with adhesion of S. aureus. Giraldez et al.37 found that lenses with a higher average surface roughness (nm at 25 μm2) adhered more viable S. epidermidis cells. Santos et al.46 found that during wear of galyfilcon A, balafilcon A, lotrafilcon A, or lotrafilcon B (non-AQUA) lenses, microbial colonization of the lens during wear was different, with colonization of balafilcon A lenses being greater than the other lens types; they speculated that the surface roughness of balafilcon A lenses contributed to their ability to be colonized by microbes during wear. González-Méijome et al.36 have published on the root-mean-square and average roughness on lenses (galyfilcon A, comfilcon A, lotrafilcon A, and balafilcon A) worn on a daily wear schedule for 2 weeks (galyfilcon A) or 1 month (other lens types). If those values were used to correlate with adhesion to worn lenses, there is still a moderate correlation between adhesion of total cells of P. aeruginosa and root-mean-square (r = −0.41; r2 = 0.17) and average (r = −0.45; r2 = 0.20) roughness of the worn lenses; strong correlations between viable cell adhesion of P. aeruginosa and root-mean-square (r = −0.83; r2 = 0.67) and average (r = −0.87; r2 = 0.75) roughness of the worn lenses. There were also moderate correlations between root-mean-square roughness and total (r = −0.41; r2 = 0.17) or viable (r = −0.35; r2 = 0.13) adhesion of S. aureus; average surface roughness and total adhesion (r = −0.32; r2 = 0.10) of S. aureus. Differences in the effects of substrate surface roughness may simply be because of the different bacterial types used in the studies. The hydrophobicity of cells of P. aeruginosa can contribute to adhesion (total cells) on a HEMA-based hydrogel contact lens; the more hydrophobic the surface of the bacteria, the more they adhered to the contact lens.47 Similar to the results from the current study, Miller and Ahearn48 found no correlation between the water content of HEMA-based hydrogel lenses and adhesion (total cells) of strains of P. aeruginosa.
The observation that adhesion of P. aeruginosa was associated with surface energy confirms data of others.49–51 Adhesion of several different bacterial types has been shown to be minimal between 20 to 30 mN/m.49–51 The results of the current analyses demonstrate that for viable adhesion of P. aeruginosa, the lowest adhesion occurred for the contact lens, balafilcon A, with the lowest surface free energy (15 nM/m). This was also generally the case for total adhesion of P. aeruginosa and total and viable adhesion of S. aureus. However, as the surface free energy results had not been measured after rinsing in PBS, the results may not be fully compatible, and further research is warranted.
Differences between the ability to adhere to contact lenses of different strains within a species/genera of bacteria have been previously reported. Fleiszig et al.52 demonstrated that adhesion of viable S. epidermidis to HEMA-based soft lenses was strain dependent. Williams et al.53 showed that adhesion to worn HEMA-based etafilcon A lenses by P. aeruginosa was strain dependant, with strain 6294 adhering in higher numbers to this lens type than strain 6206 that correlated to the findings of the current study for worn silicone hydrogel lenses.
The effect of contact lens wear on bacterial adhesion has been controversial. There have been reports that P. aeruginosa can adhere (total cells) more to worn extended wear than unworn HEMA-based soft contact lenses.54 Yet Boles et al.,27 measuring both total (using scanning electron microscopy) and viable cells of P. aeruginosa, found greater adhesion to unworn HEMA-based (etafilcon A) lenses than to lenses worn on an extended wear basis. Babaei Omali et al.40 found that after daily lens wear, when subjects used multipurpose disinfecting solution overnight, there was a significant reduction in viable cell adhesion of P. aeruginosa 6294 and S. aureus 31 to balafilcon A, but not to senofilcon A, lenses. In the present study that examined adhesion to lenses after daily disposable wear (i.e., no use of multipurpose disinfecting solution), there was an increase in viable S. aureus on senofilcon A lenses after wear, but no significant change in viable adhesion to worn balafilcon A lenses, and no significant change in viable adhesion of P. aeruginosa 6294 to either of the lens types. These differences possibly reflect the effect of adsorbed components of the multipurpose disinfecting solution to the lens during daily wear. Williams et al.53 found that adhesion of total cells was greater than adhesion of viable cells, as was found in the present study, and that lens wear generally increased total adhesion, but decreased viable adhesion, for a strain (Paer1) of P. aeruginosa to etafilcon A lenses.53 In the present study, for the silicone hydrogels, lens wear decreased viable cells adhesion to galyfilcon A, lotrafilcon B, and lotrafilcon A lenses (p < 0.05), but enhanced viable cells adhesion to balafilcon A lenses (p < 0.05). However, there were strain differences in the effect of lens wear on adhesion. Differences in effect of wear during extended vs. daily disposable wear could be because of different lens polymers that have been investigated and the effect of adsorbed tear film components. Butrus et al.54 found that addition of tear film components, such as albumin, lysozyme, and lactoferrin to a HEMA-based contact lens, increased adhesion. Although lactoferrin deposition on either HEMA-based or silicone hydrogel contact lenses can increase total adhesion, this protein can also decrease the viability of adhered P. aeruginosa.39,53 As subjects handled lenses during the removal process and did not wear gloves, it is possible that adhesion to lenses was also affected by deposition of biological material from hands onto the lens surface.
Bacterial adhesion to contact lens surfaces may be dependent on the surface properties of the bacterial cell (differences between strains) and the contact lens. Hydrophobicity of a silicone hydrogel lens surface appears to affect the ability of bacteria to adhere. Although different strains of bacteria can behave differently, overall, daily disposable contact lens wear results in increased numbers of total cells of S. aureus, but had less overall effect on total numbers of P. aeruginosa. Lens wear did not affect the viable numbers of S. aureus adhered to lenses, but did affect viable numbers of P. aeruginosa, and this was contact lens type dependent. The finding that P. aeruginosa can adhere in higher numbers (approximately 1 to 1.5 log increase) to all silicone hydrogel lenses compared with S. aureus may be clinically relevant, as P. aeruginosa is usually more frequently associated with MK than S. aureus,21,55–57 and a first step in the production of MK is likely to be adhesion to contact lens surfaces. On the other hand, there have been no reports of differences in rates of MK or other corneal infiltrative events with respect to different silicone hydrogel materials.7,58,59 Thus, it may be that the differences in adhesion of P. aeruginosa or S. aureus to various silicone hydrogel lenses of between 0.51 to 0.33 logs are perhaps not sufficient to impact the adverse event rate as a consequence of the adhesion of these bacteria to lenses.
Mark D. P. Willcox
School of Optometry and Vision Science,
University of New South Wales
Sydney, New South Wales 2052
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Keywords:© 2012 American Academy of Optometry
contact lens; bacterial adhesion; Pseudomonas; Staphylococcus