The effect of commonly used sutures on inflammation inducing pathogens – An in vitro study

Journal of Cranio-Maxillo-Facial Surgery 41 (2013) 593e597

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The effect of commonly used sutures on inflammation inducing pathogens e An in vitro study Shlomo Matalon a, Avital Kozlovsky b, Anda Kfir c, Shifra Levartovsky a, Yardena Mazor a, Hagay Slutzky a, * a b c

Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel Department of Periodontology and Osseo-Integration, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel Department of Endodontology, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel

a r t i c l e i n f o

a b s t r a c t

Article history: Paper received 7 April 2012 Accepted 20 November 2012

Introduction: Sutures are a vital part of nearly every surgical procedure designed to close and stabilize wound margins consequently allowing undisturbed wound healing. Aim: The aim of this study was to evaluate in vitro antimicrobial effect of 4 commonly used sutures. Materials and methods: The Direct Contact Test was used to evaluate the antibacterial properties of 4 types of sutures: 2 absorbable and 2 non-absorbable braided sutures, immediately or after aging for 2 or 7 days. The tested bacteria were: Staphylococcus epidermidis, Staphylococcus aureus and Pseudomonas aeruginosa. Three-way ANOVA, two-way ANOVA, one-way ANOVA and Tukey multiple comparison were used for statistical analysis. Results: The absorbable Vicryl Plus exhibited a bactericidal effect against the Staphylococcus strains, which was unaffected by aging. With P. aeruginosa, there was only an initial delay in bacterial growth. All other tested sutures did not have antibacterial effects against any of the tested bacteria (p < 0.001). Conclusions: Vicryl Plus had sustained bactericidal effect against the Staphylococcus strains but not against P. aeruginosa. None of the other sutures presented any antibacterial properties. Ó 2012 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.

Keywords: Absorbable sutures Non-absorbable braided sutures Antibacterial Triclosan

1. Introduction Surgical site infection is a major concern. It is relatively frequent, after head and neck oncological surgery and is associated with significant morbidity and mortality (Cunha et al., 2012). Sutures are a vital part of nearly every surgical procedure, designed to close and stabilize wound margins and allow undisturbed wound healing (Wikesjö et al., 1992; Minozzi et al., 2009). Most surgical infections potentially impairing wound healing are intimately related to sutures (Horan et al., 1992). In the oral cavity, sutures are placed within tissues of high vascularity in a moist bacteria rich environment with infectious potential. Bacteria and necrotic debris lodge on the suture material and invade the suture track (Selvig et al., 1998), retain infection and delay the healing cascade (Kim, 2002; Morrow and Rubinstein, 2002). The physicochemical characteristics of a suture material influence its ability to attract bacteria and consequently promote wound infection (Chu and Williams, 1984). Bacteria adhere to various types of sutures with different affinities (Katz et al., 1981). It has been shown that silk sutures, which are multi-filamentous and braided, produce * Corresponding author. Tel.: þ972 522521832; fax: þ972 36409250. E-mail addresses: [email protected], [email protected] (H. Slutzky).

a greater inflammatory reaction in the oral mucosa than monofilament sutures (Lilly et al., 1973; Racey et al., 1978; Leknes et al., 2005; Merritt et al., 1999). This reaction was attributed to the presence of bacteria in the interstices of the sutures (Morrow and Rubinstein, 2002; Parirokh et al., 2004). Therefore, it is not surprising that abscess formations have been reported more frequently with multi-filamentous, braided sutures than with monofilament sutures that elicited only a mild inflammatory tissue response (Morrow and Rubinstein, 2002). Bacteria enclosed in the interstices of the braided suture may be protected from the phagocytic activity of leucocytes, thus sustaining and prolonging an infection (Selvig et al., 1998; Österberg and Blomstedt, 1979; Österberg, 1983). Edinger and Luhr (1986) tested the influence of absorbable versus non-absorbable sutures on nerve healing indicating the advantages of absorbable sutures. Absorbable sutures, which are made of materials that are either digested by body enzymes or hydrolyzed by tissue fluids, are also susceptible to bacterial attachment and colonization (Minozzi et al., 2009; Kim, 2002). Hospital-acquired infections and antibiotic-resistant bacteria particularly methicillin-resistant Staphylococcus aureus (MRSA) can cause severe soft tissue, bone or implant infections (Warnke et al., 2009).

1010-5182/$ e see front matter Ó 2012 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jcms.2012.11.033

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Transcutaneous maxillo-facial surgery can lead to infections caused by bacteria that are commonly found on the skin such as Staphylococcus epidermidis (Spaey et al., 2005). Pseudomonas aeruginosa is a common nosocomial contaminant although it was found to be associated with severe necrotizing infection of the eyelid (Bodey et al., 1983; Steinkogler and HuberSpitzy, 1988). Microbial contamination of sutures has been shown not to be effected by daily use of 0.2% chlorhexidine solution (Sortino et al., 2008). Although controversial, the use of systemic broad-spectrum antibiotic drug therapy can significantly reduce bacterial contamination of the suture (Leknes et al., 2005). This susceptibility of sutures to infection led to the introduction of sutures treated with triclosan, a broad-spectrum antibacterial agent, which are claimed to have antibacterial properties (Rothenburger et al., 2002). The aim of this study was to evaluate in vitro the antimicrobial capacity of 4 commonly used sutures and to test whether such activity is sustained when the sutures are aged for up to 7 days in phosphate-buffered saline. 2. Materials and methods 2.1. Sutures Four commercially available suturing materials were tested: (a) braided Vicryl Plus absorbable suture (coated polyglactin 910 with triclosan, Ethicon Inc., Johnson & Johnson, New Brunswick, NJ); (b) monofilament plain gut absorbable suture (Look, Surgical Specialist Corporation, Reading, PA); (c) Polyviolene, a braided-polyester, uncoated, white, non-absorbable suture (Look, Surgical Specialist Corporation); and (d) Mersilk, a non-absorbable silk suture (Ethicon, Johnson & Johnson). The braided Vicryl Plus suture contained triclosan (2,2,4-trichloro-2-hydroxy-diphenyl ether) at a concentration of up to 150 mg/m. The other sutures did not contain any reported antibacterial agents. 2.2. Bacteria and growth conditions The three bacteria that are found most frequently in infected wound cultures (Selvig et al., 1998) were tested: S. aureus (ATCC 9144 known as the ‘Oxford Staphylococcus’), S. epidermidis (RP62A) and P. aeruginosa (ATCC 17933). The microorganisms were grown aerobically from frozen stock cultures in braineheart infusion (BHI) broth (Difco Laboratories, Detroit, MI). 2.3. Suture samples The suture samples were prepared in the shape of a flat surface continuously covered by the suture material (Fig. 1A). The suture was wrapped tightly around a small flat polypropylene plate to form a uniform layer of suture with an area of 20  0.3 mm2 (Fig. 1A). These suture-covered plates were then placed along the wall of the wells (see below) positioned to keep the suture samples away from the perpendicular light path of the plate reader, thus allowing for turbidity measurements in the wells (see below). The suture samples were tested either unaltered or after aging for 2 and 7 days while immersed in phosphate-buffered saline (PBS) that was kept at 37  C and replaced every 24 h. Each plate included 4 groups of 8 independent wells (n ¼ 32). Each experiment was repeated 3 consecutive times. 2.4. Direct Contact Test The Direct Contact Test (DCT) was performed as previously described (Weiss et al., 1996; Matalon et al., 2004). This assay is

Fig. 1. The experimental setup. (A) The suture sample: polypropylene plate wrapped with the suture. Left: Cross-section. Right: View of the flat surface. (B) The microtiter plate is held perpendicular with the wells horizontal. Left: a well with the suture sample. Center: The bacterial cell suspension is placed on the suture sample surface; the suture is in contact with the bacteria for 60 min. Right: Evaporation of the water brings bacteria into intimate contact with the suture. (C) The plate is placed horizontally, bringing the wells back to an upright position. (D) Left: The well of the experimental group A well filled with BHI broth, then vortexed gently for 2 min. Center: 15 mL from the experimental group well is then transferred into a group B well to determine the bactericidal vs. bacteriostatic properties. Right: A positive control well.

based on bringing bacteria in close contact with the tested material, followed by determination of microbial growth from bacteria that survived this contact. A 96-well, flat-bottom microtiter plate (Nunclon, Nunc, Copenhagen, Denmark) was held vertically, on its side, with the walls of the wells parallel to the floor (Fig. 1B). The suture samples were placed in the wells with the flat surface of the sample at a horizontal orientation. Ten microliters of the bacterial suspension, optical density of 650 nm, containing approximately 106 of S. aureus (5.3  107), S. epidermidis (2  108) and P. aeruginosa (1.2  107) bacterial cells in BHI were placed on the flat surface of the suture sample. The plate remained in this position for 1 h at 37  C. During this time the suspension had evaporated, thus ensuring direct contact between the microbes and the surface of the suture sample (Fig. 1B). The plate was then re-positioned horizontally with the wells in the upright position (Fig. 1C), and 235 ml of sterile BHI were added

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to each well. The plate was then incubated at 37  C in a thermostatic microplate reader (Versamax, Molecular Devices Corporation, Menlo Park, CA) and the optical density was measured in each well, at 650 nm, every half hour for 24 h. The plate was subjected to a vortex-like motion for 5 s prior to each reading to ensure a homogeneous cell suspension. When the bacteria survived the contact with the sutures a growth curve was generated by the plate reader’s software (Fig. 2). If no bacteria survived that contact, the turbidity plot remained flat (Fig. 2). 2.5. Experimental design All the experiments for each bacterium, at each time-point of the sutures, were conducted in a single 96-well plate. Each such plate included the following experimental and control groups: Group A e experimental wells (n ¼ 32, 4 groups of 8) containing the suture samples that were previously in contact with the bacterial inoculum, to which sterile BHI broth was added. After filling these wells with the BHI broth the plate was gently agitated for 2 min to release bacteria into the broth. Group B e wells for bacteriostatic vs. bactericidal effect determination (n ¼ 32, 4 groups of 8) these wells contained sterile BHI broth and were inoculated with 15 ml of the medium from the experimental group A wells, after the agitation that was mentioned above (Fig. 1D). Positive control wells (n ¼ 3) containing sterile BHI broth inoculated with the same amount of bacteria that was placed on the suture samples. Negative control wells (n ¼ 3) with no added bacteria, to verify the sterility of the BHI broth and another negative control wells (n ¼ 3) that contained suture samples with no bacteria, to ensure that the samples were not contaminated. Calibration wells (n ¼ 21), containing serial 1:5 dilutions of the positive control, to enable determination of the number of bacteria that survived the initial direct contact between sutures and bacteria. The 5-fold dilution was carried out 7 times reducing the number of S. aureus from 5.3  107 to 10.6  106, 2.12  106, 4.24  105, 84,000, 16,000, 3000, for every dilution respectively, up to 648 CFUs in the last dilution, S. epidermidis was reduced by the serial dilution from 2  108 to 2500 CFUs in the last dilution and P. aeruginosa from 1.2  107 was reduced to 153 CFUs.

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If no growth was observed in the experimental suturecontaining wells (group A) and normal growth was documented in the control wells of group B, the effect of the sutures may have been bacteriostatic. If no bacterial growth occurred in either the experimental (group A) or wells of group B, the antibacterial effect was bactericidal. 2.6. Growth curves Bacterial growth curves were generated for each well by the plate reader’s software (Fig. 2). These curves allowed for the calculation of two parameters, which were indicative of the sutureemicrobial interaction: (i) the slope of the linear ascending portion of the growth curve, expressing the bacterial growth rate and (ii) the distance of the ascending part of the growth curve from the Y-axis, which correlates to the number of viable microorganisms present in the well at time zero. This last number was determined from the growth curves generated from the calibration wells in the same plate which were inoculated with a known number of bacteria. The growth curves for each well were calculated, and a regression line was created by the plate reader’s software for the linear segment of each curve. 2.7. Statistical analysis The curves for each well were analyzed, and a regression line was created by the plate reader’s software for the linear ascending segment of the curve, the slope of this regression line was used as a parameter representing the growth rate which was used in the statistical analyses (Weiss et al., 1996; Matalon et al., 2004). The three-way ANOVA, two-way ANOVA, one-way ANOVA and Tukey multiple comparison methods were applied to this parameter. Significance level was set at p < 0.01. 3. Results The three-way ANOVA showed that time, microorganisms and the type of suture were statistically significant (p < 0.001). The post hoc analysis revealed that the effects on the two Staphylococcus strains did not differ from each other but both were significantly different from that on P. aeruginosa (p < 0.001). The effect of the Vicryl Plus suture on the staphylococci was significantly different (p < 0.001) from that of the other sutures which did not differ from each other. The experimental plates did not differ from each other, and statistical analysis was calculated to all wells containing the same suture and bacterium at the same aging time (Table 1). The braided Vicryl Plus suture proved to be bactericidal when in contact with S. aureus and S. epidermidis, either in its unaltered state or after 2 and 7 days of aging (Table 1, Fig. 2). After these bacteria were exposed to the Vicryl Plus suture, no bacterial growth occurred in either the experimental (group A wells) (Fig. 2) or the bactericidal vs. bacteriostatic group B wells (data not presented), indicating a bactericidal effect. The braided Vicryl Plus suture also had a limited antibacterial activity against P. aeruginosa (Fig. 3) but this activity was not observed after aging for 2 or 7 days. Polyviolene, plain gut and Mersilk sutures did not demonstrate an antibacterial activity against any of the tested bacteria (Figs. 2 and 3). 4. Discussion

Fig. 2. Staphylococcus epidermidis growth after contact with sutures that were aged for 7 days in PBS. Each point represents the mean optical density (O.D.) measured in 8 wells at a given time point. The slopes of the ascending part of the growth curves after bacterium exposure for the Polyviolene, plain gut and Mersilk sutures are not different from the positive control. No growth occurred when the bacterium was in contact with the Vicryl Plus suture.

Many investigators have examined the structure and chemical composition of sutures as they relate to bacterial attachment and tissue reaction. From those studies, it is clear that any suture, of natural or synthetic composition or of mono- or multi-filament

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Table 1 Bacterial growth rates according to the slopes of the linear portions of their growth curves. Staphylococcus aureus

Vicryl Plus

Staphylococcus epidermidis

Immediate

2 Days

7 Days

Immediate

2 Days

0.0002  0.00023

0.0001  0.0001

0.0003  0.00024

0.0001  0.0001

0.0001  0.0001

Pseudomonas aeruginosa 7 Days

þ

Immediate

0.0001  0.00002

0.031  0.0227

0.038  0.00346

0.031  0.004

0.038  0.0001

0.0373  0.00252

0.0313  0.00351

0.037  0.001

0.1088  0.00802

Silk

0.0234  0.00113þ

0.0271  0.00398

0.0417  0.00206

0.0410  0.00447

0.0229  0.00107

0.0376  0.00098

0.0708  0.0105

Polyviolene

0.0444  0.00678

0.033  0.00655

0.0396  0.0091

0.038  0.0051

0.0369  0.00752

0.0376  0.009

0.0963  0.01729

0.058  0.00806

0.0429  0.00618

0.0389  0.0079

0.0599  0.00873

0.0503  0.00581þ

0.0357  0.00673

0.0518  0.0209

p < 0.001

p < 0.001

p < 0.001

p < 0.001

p < 0.001

NS

Control

Plain gut

Significance p < 0.001

Each number in the table is the average ([102] standard deviation [102]) of the slope of bacterial growth in 8 separate wells in the same microtiter plate. Similar symbols indicate values which do not differ significantly (Tukey’s comparison).

structure, is susceptible to bacterial attachment and may induce an inflammatory reaction in the surrounding tissues (Morrow and Rubinstein, 2002; Leknes et al., 2005; Everett, 1970; Edlich et al., 1973). The environment of the oral cavity has great potential for a suture infection. There is a constant source of infectious pathogenic bacteria that, together with persistent moisture, allows bacteria to colonize on a suture, grow along its path and result in an infection in the healing tissues. Additionally, in the oral cavity, the sutures may be repeatedly moved by food and mastication, which may further enhance this risk. Thus, a suture material that can reduce the potential for colonization and growth of pathogenic bacteria may be preferred. In this study, the ability of several sutures to inhibit the growth of S. aureus, S. epidermidis and P. aeruginosa was studied in vitro using the Direct Contact Test. Staphylococci are the most prevalent organisms associated with device-related infections (Hirshman et al., 1984). They are also often detected in subgingival plaque samples from teeth and titanium oral implants (Salvi et al., 2008). P. aeruginosa is a common nosocomial contaminant (Bodey et al., 1983).

Fig. 3. Pseudomonas aeruginosa growth after contact with the sutures before aging. Each point represents the mean O.D. measured in 8 wells at a given time point. The slopes of the ascending part of the growth curves after bacterial exposure for the Polyviolene, plain gut and Mersilk sutures are not different from the positive control. The slope of the growth curve after contact with Vicryl Plus is less steep, indicating a partial antibacterial effect.

Our results indicate that the braided Vicryl Plus suture provided bactericidal effects against the two types of staphylococci that were used. This effect was found when the suture material was unaltered, and the suture maintained this effect after aging in PBS replaced daily for as long as seven days. The antibacterial effect is attributed to the presence of triclosan in this suture, which is one of the most effective biocides against S. aureus and S. epidermidis (Bhargava and Leonard, 1996). The lack of bactericidal effects on P. aeruginosa may be explained by the natural resistance of this bacterium to triclosan, which has been attributed to efflux pumps that are present in this bacterium (Chuanchuen et al., 2003). The present results are in agreement with those of Rothenburger et al. (2002) who used Zone of Inhibition assays to estimate the bacterial inhibitory effects of sutures. However, Zone of Inhibition assays do not provide information as to the bactericidal vs. bacteriostatic potentials of the tested materials and do not provide information about the dynamics of bacterial growth inhibition (Tobias, 1988; Atlas, 1997; Murray et al., 1995). Additionally, in the Rothenburger et al. study, the sutures were placed in an aging medium that was not replaced for 7 days; however, in the present study, the aging medium was replaced daily for 7 days, which presents a greater challenge to suture integrity and thus a more appropriate aging procedure. The results of the previous study indicate that triclosan leaches from the suture, as evidenced by its diffusion into the agar. Nevertheless, our results indicated that even after repeated daily replacement of the aging medium for 7 days, the Vicryl Plus sutures maintained a high enough concentration of triclosan to express its full bactericidal capacity against staphylococci. None of the other suture materials in this study had antibacterial effects, either when tested unaltered or after aging in PBS. Future research should expand this investigation to include additional oral pathogens, such as Porphiromonas, Prevotella and Fusobacterium strains (Otten et al., 2004; Rega et al., 2006), as these extensions were beyond the scope of the present study. The slight growth enhancement that was observed when the staphylococci were exposed to aged plain gut suture may have resulted from the release of some natural material(s) from this suture during the aging process. The design of this study did not allow for the identification or investigation of the nature of this material(s). Sutures with antimicrobial effects have been proven to be beneficial in other contexts, such as the closure of sternal surgical wounds (Fleck et al., 2007). They may also be advantageous in the oral cavity. If endodontic surgery flaps could be stabilized for an additional day or two without infection, it may make them less susceptible to mechanical dislodgement. Bone augmentation procedures as well as the placement of implants, both of which are

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adversely affected by early infection, may also benefit if suturerelated infections could be reduced. The Vicryl Plus suture may be more suitable for use in these conditions than the other suture types that were tested because of its antibacterial capacity. Nevertheless, additional in vivo and clinical studies are needed before such recommendations can be clinically adopted. 5. Conclusion Vicryl Plus had sustained bactericidal effect against the Staphylococcus strains but not against P. aeruginosa. None of the other tested sutures presented any antibacterial properties. Conflict of interest All authors disclose any financial and personal relationships with other people or organizations that could inappropriately influence (bias) their work. Disclosures The authors deny any conflicts of interest. Acknowledgments This study was supported only by The Lefco memorial fund, Tel Aviv University. References Atlas RM: Principles of microbiology, 2nd edn (international). Boston: WCB McGraw-Hill, 994e997, 1997 Bhargava HN, Leonard PA: Triclosan: application and safety. Am J Infect Control 24: 209e218, 1996 Bodey GP, Boliver R, Fainstein V, Jadeja L: Infections caused by Pseudomonas aeruginosa. J Clinic Infect Dis 5: 279e313, 1983 Chu CC, Williams DF: Effects of physical configuration and chemicals structure of suture materials on bacterial adhesion. A possible link to wound infection. Am J Surg 147: 197e204, 1984 Chuanchuen R, Karkhoff-Schweizer RR, Schweizer HP: High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am J Infect Control 31: 124e171, 2003 Cunha TF, Soares Melancia TA, Zagalo Fernandes Ribeiro CM, Almeida de Brito JA, Abreu Miguel SS, André Abreu Esteves Bogalhão do Casal D: Risk factors for surgical site infection in cervico-facial oncological surgery. J Craniomaxillofac Surg 40: 443e448, 2012 Edinger D, Luhr HG: Free autologous nerve grafting-comparison of suture materials. J Maxillofac Surg 14: 227e230, 1986 Edlich RF, Panek PH, Rodeheaver GT, Turnbull VG, Kurtz LD, Edgerton MT: Physical and chemical configuration of sutures in the development of surgical infection. Ann Surg 177: 679e688, 1973 Everett WG: Suture materials in general surgery. Prog Surg 8: 14e37, 1970 Hirshman HP, Schurman DJ, Kajiyama G: Penetration of Staphylococcus aureus into sutured wounds. J Orthop Res 2: 269e271, 1984 Fleck T, Moidl R, Blacky A, Fleck M, Wolner E, Grabenwoger M, et al: Triclosancoated sutures for the reduction of sternal wound infections: economic considerations. Ann Thorac Surg 84: 232e236, 2007

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