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Infection prevention in shoulder surgery.

Postoperative infections after shoulder surgery are a serious cause of patient morbidity and rising healthcare expenditures. Although the reported rates of infection after shoulder surgery are relatively low, ranging between 0.4% to 5%, (1,2) these infections often require revision surgery, longer hospital stays, and an increased use of antibiotics. Furthermore, these patients often have poorer results than their matched counterparts who have uncomplicated courses. (3) Additionally, with the institution of the Affordable Care Act, postoperative complications, such as infections, may not be reimbursed, placing the burden of caring for infections upon the physician, hospital, or accountable care organization, further necessitating the need for improved infection prevention. Reducing the economic burden of treating postoperative shoulder infections depends on developing clinical practice guidelines, such as those used for hip and knee arthroplasty, and incentivizing innovations in infection prevention. (4) We will examine the current literature regarding infection prevention in shoulder surgery, with special attention directed towards the prevention of Propionibacterium acnes infection.

Infective Organisms

As stated previously, the rate of infection after shoulder surgery remains low. The common infective organisms are typically coagulase-negative staphylococcal species, such as S. epidermidis and P. acnes, both of which are part of the normal skin flora. In a study by Maraceck and colleagues, the skin flora of axilla in male subjects prior to surgical preparation demonstrated the presence of coagulase-negative staphylococcal species and P acnes in 72.9% and 72.4% cultures, respectively. This contrasts to the presence of Staphylococcus aureus in only 4.7% of the cultures taken prior to surgical preparation. (5)

P acnes and coagulase-negative staphylococcal species, such as S. epidermidis, are believed to be commensal organisms of the human skin microbiome. These two species help to fight other pathogens, such as S. aureus, and maintain homeostasis of the skin microbiome, even maintaining a biologic balance between each other when one species overgrows. (6,7) P. acnes, in particular, acts as a chimeric organism. This Gram-positive, saprophytic organism is intimately associated with sebaceous glands. It is an anaerobic organism but is aerotolerant, even expressing the ability to employ oxidative phosphorylation for energy conservation. It is present throughout the body, notably the gut, where, just as it does on the skin, it functions in modulation of the microbiota and immunomodulation.

However, P. acnes can act as an opportunistic pathogen, causing inflammatory responses by secreting a host-tissue component that degrades enzymes such as cytotoxic cAMP factors. (7) This can be seen in disease processes, such as acne vulgaris and shoulder infections, and there has even been some speculation that it has some involvement in the pathogenesis of prostate cancer. This organism, which was historically dismissed as a contaminant that did not necessitate treatment in revision shoulder surgery, appears to significantly contribute to shoulder pain, stiffness, and component loosening without displaying the overt signs of periprosthetic infection. (8) It is poorly understood why P. acnes exhibits parasitic properties, but it appears that certain strains, or phylotypes, exhibit these inflammatory properties more so than do others. The inflammatory response exhibited by P. acnes certainly has some relation to the host cell type-specific response, as well. (7) Additionally, P. acnes'ability to form an antibiotic resistant biofilm enables its ability to be eradicated unless prosthesis exchange and prompt antibiotic therapy are initiated. (9,10) Further research is currently being performed on P acnes in regards to both its mutualistic and parasitic properties. (7)

Staphylococcus epidermidis, such as P. acnes, has evolved over time with the human host. (6,7) Similar to P. acnes, it is considered a mutualistic part of the skin flora, acting against more pathogenic organisms on the skin, such as S. aureus, and on P. acnes in instances of overgrowth, such as acne vulgaris. (6) However, this particular organism is considered an opportunistic pathogen when it breaches the skin surface. It is the leading cause of hospital-acquired infections and bacteremia, mostly associated with medical device use in immune-compromised patients. (7) Similar to P. acnes, its pathogenesis relies on the creation of multilayered biofilms that allow it to attach to foreign bodies and host tissue enabling it to resist to host clearance. Some strains even contain the methicillin resistance gene, mecA, further enabling its pathogenic abilities. (7)

Risk Factors

Risk factors for deep infection following shoulder arthroplasty include patient sex, age, indication for the procedure, type of arthroplasty performed, and number of procedures performed on the shoulder prior to arthroplasty. (11,12) In a retrospective cohort study of 3,906 subjects undergoing primary shoulder arthroplasty, Richards and colleagues (11) found no association with deep infection rate and ASA score, BMI, diabetes mellitus, or race. However, this group reported that with every one-year increase in age, a 5% lower risk of infection was observed. In parallel to many other studies, men were 2.59 times more likely to have a postoperative deep infection following arthroplasty. Arthroplasties performed in the setting of trauma were 2.98 times more likely to develop postoperative infection. Additionally, patients undergoing reverse total shoulder arthroplasty had a 6.11 greater risk of infection compared to those undergoing primary unconstrained total shoulder arthroplasty. (11) Contrary to these findings, in a retrospective study following 814 shoulder arthroplasties, Florschutz and associates (12) found no significant difference in infection rates when comparing primary reverse total shoulder arthroplasty to primary anatomic total shoulder arthroplasty. However, they found that subjects who had previously undergone non-arthroplasty procedures prior to initial anatomic and reverse total arthroplasties had a 3.35 and 4.8 higher risk of infection, respectively, compared to subjects who had never undergone non-arthroplasty procedures prior to their index arthroplasty. (12)

General Considerations

Many considerations have been examined in regards to prevention of orthopaedic infection. Multiple studies have shown that decreased operative time, operating room traffic, and room noise have been effective means of reducing orthopaedic infections. (13-18) Additionally, Dalstrom and colleagues demonstrated a time-dependence in regards to the length of time that operating-room trays were opened and the rate at which they became contaminated. (13) While wound irrigation conceptually would seem to reduce infection rates, there have been conflicting results in regards to surgical site infection prevention. (14,15)

Hand washing has been reported as the single most effective measure for minimizing infection. (16) In comparing three traditional types of scrub, both alcohol and chlorhexidine have proved to be more potent than povidone-iodine scrubs in reducing CFUs. Alcohol has proved to be more potent in reducing CFUs; however, chlorhexidine has the ability to bind longer to the skin. In a study by Parienti and coworkers, chlorhexidine prevented the return to normal bacterial levels for up to 6 hours post scrub. In regards to a traditional scrub versus the used of aqueous rubs, a randomized control trial in France in 2002 demonstrated no difference in infection rates when comparing a 5-minute traditional chlorhexidine scrub to the use of an aqueous dry scrub after nonsterile hand washing. (17) In addition to hand washing, frequent glove changing, especially after draping takes place, has been found to significantly reduce the rate of surgical site infections. (18) Multiple studies have shown that surgical exhaust gowns provide a significant decrease in bacterial colony forming units; however, this has not correlated with a decrease in the effectiveness of preventing wound contamination. (19,20)

Skin Preparation

Multiple studies have demonstrated the improved efficacy of surgical site preparation with chlorhexidine, compared to iodine containing scrubs. (21-23) Saltzman and colleagues cultured the skin immediately after skin preparation and found the culture positive rate to be much lower with chlorhexidine (7%) compared to povidone-iodine scrub (31%); however, neither agent proved to be more effective over the other in regards to elimination of P. acnes from the shoulder region. (21) The reason for chlorhexidine's ineffectiveness at eliminating P. acnes might be due to the fact that this organism resides primarily in the dermal layer. Lee and coworkers performed dermal punch biopsies in 10 healthy male individuals after skin preparation with chlorhexidine gluconate and found 70% of these individuals to be positive for P. acnes. (24) Sethi and associates studied subjects undergoing index shoulder arthroscopies to evaluate for the presence of P acnes. (25) After performing a skin preparation, which included using a scrub brush containing 3.3% chloroxylenol followed with three applications of 2% chlorhexidine gluconate, skin swab cultures were taken before skin incision and at the conclusion of the operation. Three intraoperative deep tissue cultures were taken, as well. Skin cultures were positive for P acnes in 15.8% of the subjects immediately following skin preparation. This number of subjects increased to 40.4% by the end of the operation. Of all 57 subjects in the study, 32 subjects (56%) had at least one positive culture for P acnes. (25)

Hudek and colleagues took skin, superficial, and deep tissue samples in 118 subjects undergoing their index open shoulder procedure. Of these 118 subjects, 43 (36.4%) had at least one positive culture for P acnes. (26) Two recent prospective studies have demonstrated the incidence of P acnes in open shoulder surgery and shoulder arthroscopy. In a study by Mook and coworkers, after performing skin preparation with a scrub brush filled with 4% chlorhexidine gluconate followed by cleaning with an ethyl-isopropyl alcohol solution and final preparation with 2% chlorhexidine gluconate and 70% isopropyl alcohol paint, three periscapular tissue cultures were taken in patients undergoing an open deltopectoral approach. Of 82 patients who had not previously undergone shoulder surgery, the cultures of 14 (17.1%) were positive for P acnes. (27)

Chuang and associates (28) found similar results in 51 patients undergoing index shoulder arthroscopy. These patients underwent skin preparation with a 5-minute scrub with 4% wt/vol chlorhexidine solution followed by application of 2% chlorhexidine gluconate and 70% isopropyl alcohol. After labral or rotator cuff repair was performed, deep tissue cultures were taken from around the surgical site. Ten of 51 (19.6%) deep tissue cultures were positive for P acnes. (28) While standard skin preparation has not proved to provide adequate coverage for P. acnes, using a standard benzoyl peroxide based preparation has been shown to minimize the rate of positive cultures in both the skin and deep tissues. In a study by Sabetta and colleagues, 50 patients were treated with topical 5% benzoyl peroxide cream for 48 hours prior to undergoing arthroscopic shoulder surgery. These patients then underwent skin preparation with a 3.3% chloroxylenol scrub and 2% chlorhexidine paint. Skin cultures were taken before and after incision. Additionally, joint aspirates and deep cultures were taken. Twenty-five of 400 (6.25%) skin cultures were positive after skin preparation. This number percentage increased to 10% at the conclusion of surgery.

Only 6% of deep tissue cultures and 4% of joint aspirates were positive. This culture positive rate was equivalent with the air control swab. Additionally, there was no difference in rates of positive cultures found in males versus females, and none of these patients were displaying signs or symptoms of shoulder infection at 9-month follow-up. (29)

Adhesive Drapes

While the idea behind applying adhesive drapes, especially those impregnated with iodophor, to the skin after surgical site preparation would seem to reduce infection rate, multiple studies have not proven this to be true. (30)

Preoperative Hair Shaving

Similar to the use of adhesive drapes, preoperative hair shaving would seem to reduce the bacterial load around surgical sites; however, at least one study has proved to be quite the contrary. Maracek and colleagues found that removal of axillary hair had no effect on the bacterial burden of P acnes. Additionally, clipped axillae had a higher total bacterial burden than did unclipped axillae. (5)

Incision Site

While both Saltzman and coworkers (21) and Lee and associates (24) both showed the ineffectiveness of surgical skin preparation, Saltzman and coworkers (21) and Hudek and colleagues (26) further compared the rate of culture positivity at certain aspects of the shoulder. Saltzman found that after skin preparation with ChloraPrep[R], bacteria grew on the culture from 10% of the specimens taken from either an anterior or posterior arthroscopic portal site. (21) Hudek and colleagues compared standard approaches to open shoulder procedures and found that the relative risk for obtaining a positive P acnes culture was two-fold greater at the incision site for the anterolateral approach than for the deltopectoral approach. (26)

Antibiotics

There have been no studies related to infection in shoulder surgery and the administration of prophylactic antibiotics; however, multiple studies in the total joint arthroplasty literature have demonstrated the effectiveness of preoperative administration of cefazolin or cefuroxime prior to incision. Vancomycin is recommended for use in patients with prior history of methicillin resistance Staphylococcus aureus infection or colonization. (31,32) While many shoulder arthroplasties are performed with a press-fit technique rather than with bone cement, Nowinski and coworkers (33) studied the effect of the use of antibiotic-loaded cement and its effect on deep infection. This multi-institutional, retrospective study compared the infection rate in 265 reverse shoulder arthroplasties that had humeral component fixation with standard bone cement to 236 shoulders that had humeral component fixation with cement impregnated with tobramycin, gentamycin, or vancomycin/tobramycin. At an average follow-up of 37 months, the infection rate in the standard cement group was 3.0% (8/265) versus 0% in the antibiotic-impregnated cement group. There was no evidence of osteolysis, prosthesis loosening, or altered biomechanical properties in the antibiotic-impregnated group. (33) Lovallo and associates (34) retrospectively looked at the effect of intra-articular gentamicin injection into the glenohumeral joint following total shoulder arthroplasties. The infection rate in those receiving the injection was 0.29% (1/343 patients) versus 3% (5/164 patients) in those who did not receive a postoperative intraarticular injection. (34)

Conclusion

Infection following shoulder surgery is a devastating complication. While previous reports have shown that the most common organisms found in deep infection are Gram-positive aerobic bacteria, multiple recent studies have demonstrated that P. acnes may be more prevalent. Many studies in the orthopaedic literature have shown that hand washing, decreasing operative time, routine glove changing, minimizing operating room traffic, and covering instruments can decrease the risk of deep infection. And while chlorhexidine appears to be the most efficacious skin preparation agent, it still has minimal effect on eradication of P. acnes from the surgical site. Preoperative topical applications of benzoyl peroxide have shown promise in decreasing the rate of P. acnes culture positivity. Hair clipping and the use of adhesive drapes may have little effect on decreasing the incidence of deep infection. The relative risk of obtaining a positive P. acnes culture is twice as high with the anterolateral approach than with the deltopectoral approach. The use of antibiotic impregnated cement and intra-articular gentamicin immediately postoperatively seem to be an effective means of preventing deep infection. As suggested by Lee and colleagues, further strategies need to be developed for preventing Priopionibacterium contamination of surgical wounds by addressing the bacteria both on and in the skin at the surgical site. (24)

Conflict of Interest Statement

Daniel J. Hackett, Jr., M.D., has no conflict of interest to report. Lynn A. Crosby, M.D., is a consultant for and receives royalties from Exactech, Inc., Gainesville, Florida.

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(33.) Nowinski RJ, Gillespie RJ, Shishani Y, et al. Antibiotic-loaded bone cement reduces deep infection rates for primary reverse total shoulder arthroplasty: a retrospective, cohort study of 501 shoulders. J Shoulder Elbow Surg. 2012 Mar; 21(3):324-8.

(34.) Lovallo J, Helming J, Jafari SM, et al. Intraoperative intra-articular injection of gentamicin: will it decrease the risk of infection in total shoulder arthroplasty? J Shoulder Elbow Surg. 2014 Sep; 23(9):1272-6.

Daniel J. Hackett, Jr., M.D., Department of Orthopaedic Surgery, Georgia Regents University, Augusta, Georgia. Lynn A. Crosby, M.D., Department of Orthopaedic Surgery, Georgia Regents University, Augusta, Georgia.

Correspondence: LynnA. Crosby, M.D., 1120 15th Street, Augusta, Georgia 30912; lycrosby@gru.edu.
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Author:Hackett, Daniel J., Jr.; Crosby, Lynn A.
Publication:Bulletin of the NYU Hospital for Joint Diseases
Article Type:Report
Date:Oct 1, 2015
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