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Prevention of Periprosthetic Joint Infection: What Are the Effective Strategies? Snir Heller, MD1

Javad Parvizi, MD, FRCS1

1 Department of Orthopaedics, Rothman Institute, Philadelphia,

Pennsylvania J Knee Surg 2014;27:251–258.

Abstract

Keywords

► periprosthetic joint infection ► surgical site infection ► total knee arthroplasty ► prevention

Address for correspondence Javad Parvizi, MD, FRCS, Department of Orthopaedics, Rothman Institute of Orthopaedics at Thomas Jefferson Hospital, 925 Chestnut Street, Philadelphia, PA 19107 (e-mail: [email protected]).

Periprosthetic joint infection (PJI) following total knee arthroplasty is a major burden for patients and health systems. Prevention of this challenging complication through implementation of effective strategies should be a priority. These strategies should encompass various levels of patient care. Multiple modifiable risk factors such as uncontrolled hyperglycemia, obesity, smoking, substance abuse, and nasal colonization with Staphylococcus aureus have been described for PJI. Preoperative recognition and mitigation of these risk factors along with optimization of nonmodifiable risk factors such as kidney, liver, or immune system insufficiency can considerably decrease the risk of PJI. A comprehensive perioperative protocol should involve optimization of the operative environment to reduce the number of bacteria and particulates in the air. Several surgical and nonsurgical details of intraoperative care such as maintenance of normothermia, skin preparation, surgical field irrigation, wound closure, and duration of surgical and anesthetic procedure can influence the occurrence of PJI. Prophylactic perioperative antibiotic administration is probably one of the most important strategies in preventing PJI. Implementation of surgical safety checklist can diminish the risk of perioperative complications, particularly surgical site infection. Controversy regarding efficacy, efficiency, and optimization of some preventive measures continues to exist due to inconsistency or inadequacy of available evidence. Novel research has focused on designing PJI-resistant implants and developing vaccines that target molecule components with major role in the process of bacterial adhesion to the implant or periprosthetic tissues.

Periprosthetic joint infection (PJI) has considerable impact on the physical and emotional health of patients. It requires significant financial and logistic resources and is a substantial burden to the health systems and society. Prevention should be the prime concern in confronting such a major challenge. It should consist of identifying and mitigating risk factors and implementing effective prophylactic strategies in the routine surgical and nonsurgical care of patients undergoing total joint arthroplasty (TJA). Though multiple modifiable and nonmodifiable risk factors have been described for PJI, the absence of known risk factors does not guarantee protection

against PJI. The presence of nonmodifiable risk factors such as organ insufficiency or persistent nasal colonization with Staphylococcus aureus despite prior attempts for decolonization is an unfortunate situation over which orthopedic surgeons have no control. However, inadequate optimization of modifiable risk factors such as uncontrolled hyperglycemia and/or diabetes, malnutrition, obesity, and smoking is less tolerable. Diverse strategies are currently practiced to prevent septic complications of surgical wounds in the early postoperative period and occurrence of PJI in the long-term period. This

received January 30, 2014 accepted after revision February 24, 2014 published online May 3, 2014

Copyright © 2014 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.

DOI http://dx.doi.org/ 10.1055/s-0034-1376332. ISSN 1538-8506.

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Pouya Alijanipour, MD1

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diversity of presentation is an obstacle for establishing standards for comparative investigation. The main challenges are determining the most efficient and effective strategies for preventing PJI and how to incorporate them into current practice. This article attempts to assist orthopedic surgeons for confronting such challenges.

Patient-Related Factors Uncontrolled Hyperglycemia The proposed concept of “diabetic disadvantage”1 is based on several observations demonstrating the association of hyperglycemia with increased incidence of postoperative complications and higher mortality following TJA.2,3 Better glycemic control lowers the rate of perioperative complications4 and the presence of diabetes raises the odds of developing PJI.5–7 Hyperglycemia is correlated with impairment in various aspects of defense against bacteria such as bactericidal activity of neutrophils, as well as humeral and cell-mediated immunity.8 Hyperglycemia also impairs collagen synthesis, and the rate of surgical wound-related complications in diabetic patients undergoing TKA have been reported to be as high as 12%.9,10 Metabolic derangement due to fasting for the surgical procedure can be challenging and may prolong hospital stay.11 An appropriate parameter with a precise threshold that would be able to distinguish high-risk patients has yet to be determined. Point-of-care measures, such as self-monitoring blood glucose or perioperative blood levels, represent current glycemic status. These parameters have been shown to be correlated with PJI due to the immediate adverse effects of hyperglycemia.2,12 However, they do not provide information regarding physiologic impairments that happen during extended periods of uncontrolled hyperglycemia. Glycosylated hemoglobin (HbA1c) indicates the glycemic control over the last 3 months, but levels may be affected by momentary peaks in glucose level. On the contrary, a history of ketoacidosis or hyperosmolar diabetic coma represents previous decompensation and do not necessarily imply subsequent suboptimal condition of the patient. End-organ damage, as an indicator of chronically uncontrolled diabetes,13 happens in late stages and is not an appropriate risk index for the majority of diabetic patients. For perioperative glycemic control for TJA, recent guidelines from American Diabetes Association and Endocrine Society recommended an average pre- and postprandial glucose levels of 90 to 130 and less than 180 mg/dL, respectively, and HbA1c level below 7% as glycemic targets for elective surgeries.4,14

Malnutrition Optimal nutritional status favors better surgical outcome.15 Adequate nutritional reserve can mitigate the adverse effects from the postsurgical catabolic state that is common after major surgery such as TJA.16 Moreover, malnutrition has adverse influence on local and systemic defenses against pathogenic bacteria and impairs collagen and proteoglycan synthesis required for wound healing. Risk of surgical wound complications was observed to increase in patients with perioperative nutritional depletion. 17,18 Moreover, malnutrition was associated with prolonged The Journal of Knee Surgery

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rehabilitation recovery and longer postoperative in-hospital stay.16–19 Common indices for malnutrition are serum albumin less that 3.5 g/dL, serum transferrin less than 200 mg/dL, and total lymphocyte count less than 1,500/mm3, but they only indicate protein deficiency and do not represent calorie and vitamin deficiency that can potentially be present in patients undergoing TJA.20

Obesity Studies with different thresholds for body mass index (BMI) have found obesity to be a risk factor of PJI.21–23 However, BMI over 35 kg/m2 seems to constitute a challenging scenario, as it has been shown to increase the risk of infection following TKA by 6.7 times.24 Associated comorbidities in obese patients, such as poor nutritional status and diabetes, are associated with delayed postoperative recovery and increased risk of perioperative events, particularly surgical wound-related complications.25,26 The local defense and repair mechanisms at the site of surgery can be impaired due to metabolic derangements and suboptimal tension of oxygen in the bulky peri-incisional fatty tissue.27 Increased mechanical tension at the site of incision can cause wound dehiscence, and extensive dissection during surgery can facilitate formation of hematoma or seroma and prolonged wound drainage.28 Moreover, intraoperative technical challenges in obese patients may prolong surgical time and indirectly increase the risk of PJI. Obese patients should be optimized in terms of their metabolic status before considering TJA. Nonsurgical weight reduction strategies, such as diet and activity modification, and bariatric surgery can be considered.29 However, rapid excessive weight loss is not desirable in the perioperative period because it may induce a catabolic state. Furthermore, doses of prophylactic antibiotics in obese patients should be meticulously adjusted, as inadequate dosage of perioperative antibiotics is not uncommon in obese patients.30

Smoking Smoking impairs collagen synthesis and maturation in subcutaneous tissue.31 Moreover, it can result in poor oxygen supply to the surgical site due to nicotine-induced vasoconstriction, shift of oxyhemoglobin dissociation curve, and microthrombus formation by abnormal platelet aggregation. Heavy smoking (more than one pack per day) was significantly associated with PJI and other postoperative complications.32 Preoperative screening for tobacco use and offering strategies to quit or decrease smoking are highly recommended. Current smokers are at higher risk of PJI than exsmokers33 and cessation programs as early as 6 to 8 weeks before operation have been able to decrease the incidence of perioperative complications.34,35

Substance Abuse Excessive alcohol consumption, as defined by more than 40 units (400 g of pure alcohol) per week, was reported to be associated with increased risk of both infectious and noninfectious postoperative complications.36,37 The suggested mechanisms are immunosuppression, preclinical cardiac

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Ongoing Organ Disease/Failure Elective TJA performed for patients with chronic visceral disorders, such as renal insufficiency with or without dialysis, asymptomatic hepatitis C, and hepatic insufficiency, are associated with significant mortality and morbidity including PJI.41–44 Before TJA, these conditions should be thoroughly evaluated and optimized based on goals individualized for each patient. Patients with immune system insufficiency are at increased risk of perioperative complications and PJI. Examples are human immunodeficiency virus (HIV) infection,40,45 chronic immunosuppressive therapy due to organ transplant46 and inflammatory disorders,47 and metastatic cancers. These patients are also at increased risk for late PJI; thus after the procedure, these patients should still continue to receive meticulous care to maintain their immune status at an optimal level. Protocols of prolonged prophylactic antibiotic administration have been described,48,49 but there have been no comparative studies to prove their efficacy. For HIVinfected patients, CD4 counts greater than 400 and an undetected viral load may be considered as appropriate candidates for TJA.50 For patients with rheumatoid arthritis, preoperative stoppage of certain immunosuppressive medications has been recommended for at least three to five times of the half-life of each individual medication, but such plans should be individualized based on patients’ conditions.51

Staphylococcus aureus Screening and Decolonization According to a national U.S. survey, nasal colonization with S. aureus declined from 32 to 28%, while the prevalence of methicillin-resistant S. aureus (MRSA) increased from 0.8 to 1.5% from 2001 to 2004.52 S. aureus carriers are at higher risk for surgical site infection (SSI) and other septic complications.53 A recent meta-analysis assessing the efficacy of nasal decolonization for prevention of SSI after orthopedic and cardiac surgeries showed significant protective effect of nasal decolonization against SSI due to methicillin-sensitive S. aureus or MRSA.54 Despite encouraging reports of efficacy of mupirocin ointment in reducing nosocomial S. aureus infections,55 concerns have been raised regarding bacteria resistance associated with routine use of mupirocin.56,57 However, a Cochrane systematic review did not confirm this association.55 A cost analysis study showed treatment with mupirocin, either with or without screening, was costeffective compared with no decolonization.58 Nevertheless, current guidelines do not recommend routine screening for nasal colonization with S. aureus due to lack of sufficient evidence.59 According to a prospective study, 33% of preoperatively decolonized patients were recolonized with S. aureus

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15 months after TJA.60 However, there is no evidence that colonization with S. aureus after TJA is a risk factor for late PJI, and therefore no treatment is advised for S. aureus carriers after TJA (►Table 1).

Operating Room Environment Postoperative SSIs are believed to occur via bacterial inoculation of the wound at the time of surgery through open pathways to the deep tissues.61 Particles that are shed in the operating room (OR) environment are the predominant source of contamination by airborne bacteria.62 The number of airborne bacteria around the wound has been correlated with the incidence of SSI and particulate counting has been suggested for real-time monitoring of wound contamination.61 Therefore, every effort to reduce the number of particles and bacteria in the OR would be beneficial. Laminar flow systems were designed to reduce particulate load in OR, but the evidence regarding their efficacy in lowering incidence of SSI is inconsistent and conflictive,63–65 probably due to the technical complexity of their use and maintenance. Similarly, use of a body exhaust suit is controversial and although it has been supported by earlier reports, the results of recently published retrospective studies do not favor its use.65,66 The use of ultraviolet lights can significantly

Table 1 Currently recommended values for preoperative optimization of patients Preventive parameter

Suggested threshold

Preprandial glucose levels

80–130 mg/dL

Postprandial glucose levels

180 mg/dL

Hemoglobin A1c

7%

Serum albumin level

3.5 g/dL

Serum transferrin

200 mg/dL

Total lymphocyte count

1,500/mm3

BMI

35 kg/m2

Heavy smokinga

Cessation 6–8 wk before surgery

Excessive alcohol consumptionb

Abstinence at least 4 wk before surgery

HIV-positive patients

CD4 counts > 400 cells/mm3 and undetected viral load

Immunosuppressive medications in rheumatoid arthritis and other inflammatory disorders

Preoperative stoppage at least 3–5 times of the half-life of each individual medication before surgeryc

Abbreviations: BMI, body mass index; CD4, cluster of differentiation 4; HIV, human immunodeficiency virus; hemoglobin A1c, glycosylated hemoglobin. a Defined as more than one pack per day. b Defined as more than 40 units or 400 g of pure alcohol per week. c Plans for drug stoppage should be individualized based on each patient’s conditions. The Journal of Knee Surgery

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insufficiency, hemostatic imbalance, and exaggerated response to surgical stress.38 A period of at least 4 weeks of abstinence has been suggested to be necessary to reverse pathophysiologic changes that increase the risk of postsurgical morbidity in alcohol consumers.39 Intravenous drug abusers are at obvious risk for PJI and other infectious complications, particularly through hematogenous spread of bacteria.40 Elective joint replacement for these patients is not recommended.

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decrease the number of viable bacteria, yet is not recommended due to its potential harm for OR personnel.67 OR personnel should have adequate insight regarding their role in bacterial shedding. The number of OR personnel and the amount of OR traffic should be kept to minimum as both factors have been associated with increased air contamination.68

Intraoperative Strategies Systematic performing of a “surgical safety checklist ” before incision has been shown by large-size prospective studies to decrease the number of postoperative complications in general and SSI in particular.69,70 This strategy improves interpersonal communication and ensures fulfillment of important prophylactic measures such as adequate timing of antibiotics.71 There is evidence from nonorthopedic literature demonstrating the association between maintenance of normothermia during the surgery and decrease in the incidence of SSI.72 Forced air warming technology has been suggested to maintain normothermia, and despite concerns regarding possibility of bacterial air contamination and interference with laminar flow systems, no clinical study has shown association with forced air warming and SSI.73,74 Hair removal should be done if hair at incision site interferes with the procedure.75 It should be done in the hospital, yet outside of the OR and as close to the time of surgery as possible. Randomized prospective studies support the use of clippers compared with razors to reduce the incidence of SSI.76 A considerable variety of methods for effective skin preparation exists and preference for one antiseptic solution over another might be less relevant.77,78 However, the use of alcohol should be part of the antiseptic skin preparation regimen, as it acts rapidly and effectively at eradicating bacteria. Nevertheless, alcohol as a sole agent acts for a short duration and its antiseptic effect disappears within minutes.75 Clinical outcome-based evidence regarding draping is lacking, but experimental evidence shows that disposable, nonwoven drapes are more resistant to bacterial penetration than reusable woven drapes.79 The use of sticky U-drapes is a wise practice to implement for isolating the perineum. Incise drapes impregnated with antiseptic solutions should not substitute skin preparation protocols. Lack of well-designed and adequately powered prospective studies has caused some confusion regarding their clinical efficacy.80 Appropriate methods of incise draping should prevent detachment from skin, which can significantly increase skin contamination.81 It has been shown that the type of antiseptic solution can affect adhesive properties of incise draping.82 Irrigation is an effective strategy to prevent surgical field contamination. The minimum advantage of irrigation is physical removal of the particulates. However, details such as the type and content of irrigation solution, volume of irrigation solution, and delivery system (low pressure vs. high pressure) are interrelated factors and defining an ideal irrigation protocol is difficult. Moreover, evidence for irrigation in clean-contaminated or contaminated surgical procedures might not be applicable to clean procedures. Detergents such The Journal of Knee Surgery

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as castile soap or benzalkonium chloride can be used as irrigation solutions. They effectively disrupt hydrophobic and electrostatic forces that facilitate bacterial attachment to soft tissues and bone.83 Strong evidence for the benefit of using diluted betadine as an irrigation solution before closure of surgical wound is lacking. However, no deleterious influence on wound healing or any other major adverse effect has been associated with their use.84 Both clinical85 and experimental evidence86 do not support adding antibiotics to the irrigation solution. Using a pulsatile lavage system, irrigation with more than 4 L normal saline did not remove further particulates (bigger than 1 µm).87 High-pressure pulsatile lavage may have potential benefits of being time saving and effective for removing necrotic tissue and debris, and may offer better mechanical stability for cemented arthroplasty by allowing better cement penetration in cancellous bone tissue.88,89 However, concerns exist regarding mechanical damage to the tissues, propagation of bacteria into deeper layers of tissue, and negative influence on healing and new bone formation.90,91 As for wound closure, there is no strong evidence demonstrating clear superiority of one method of closure over the others. Most of the studies were underpowered, did not define SSI adequately, and did not consider the influence of host factors for wound healing. However, one meta-analysis demonstrated that there was a significantly higher risk of SSI following closure with staples compared with sutures.92 Closure of surgical wounds in TKA requires adequate strength to overcome mechanical tension. However, excessively tight closure may potentiate skin necrosis. As for operative time, a statistically significant link between prolonged surgical time and increased incidence of SSI has been described in multiple studies.5,99 Prolonged surgical time is part of National Nosocomial Infections Surveillance risk index for PJI.66 However, it is difficult to determine whether there is cause–effect relationship between surgical time and PJI, or surgical time is a surrogate for other confounding factors including the complexity of surgical procedure, an inexperienced surgical team, an inadequate optimization of OR standard protocols, or intraoperative surgical or anesthetic complications. While every single detail of the surgical procedure should be approached with meticulous care, minimization of duration of surgery is an important goal.

Perioperative Antibiotic Administration Prophylactic perioperative antibiotic administration has been shown to be the most important factor in preventing PJI. First- or second-generation cephalosporins are effective against most common pathogens, have good bioavailability, and are cost-effective, and therefore should be routinely used.93 Alternatively, vancomycin can be administrated in cases of drug sensitivity to cephalosporins. Exposure to vancomycin may result in the emergence of vancomycin intermediate S. aureus or vancomycin resistance S. aureus; hence, unnecessary usage should be avoided.94 Prophylaxis with vancomycin is indicated for high-risk patients, such as known MRSA carriers, nursing home residents, and health

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care professionals. These antibiotics should be administrated within 1 hour before surgery to reach the minimal inhibitory concentration in the end organs during the operation.95 A second dose should be administrated when the surgery prolongs beyond the half-life time of the antibiotics or when there is excessive blood loss. The duration of treatment should not exceed 24 hours, as more prolonged treatment has no additive effect and may facilitate bacterial resistance to antibiotics. While addition of antibiotics to cement for total hip arthroplasty has been shown to considerably reduce the risk of PJI,96,97 the data regarding TKA are inconsistent and less conclusive.98,99

Blood Transfusion Allogeneic blood transfusion has been shown to be an independent risk factor for PJI, potentially due to its modulating effects on the immune system.100 The risk for PJI increases as the number of transfused units increases.101 Hence, all efforts should be made to minimize blood transfusion. Potential effective strategies can be correction of preexisting anemia102 and minimization of blood loss via meticulous hemostasis, neuraxial (rather than general) anesthesia, and administration of tranexamic acid.103,104 The decision of blood transfusion should be judicious, based on clinical symptoms rather than on hemoglobin levels.

Prevention of Late Periprosthetic Joint infection Patients after TJA may be at risk for late PJI due to transient bacteremia. Prophylactic antibiotic treatment has been supported by the American Academy of Orthopedic Surgeons in cases of anticipated bacteremia, such as dental care and other selected invasive procedures.105 Although there is evidence for bacteremia during dental procedures,106,107 the actual risk for PJI following dental procedure is unclear. Current evidence does not confirm efficacy of routine antibiotic prophylaxis before dental procedures.108 Appropriate oral hygiene should be maintained in all patients to reduce the risk of transient bacteremia following daily tooth care.109 Certain upper and lower gastrointestinal (GI) procedures as well as genitourinary (GU) endoscopic procedures can also be associated with transient bacteremia. There is no direct evidence regarding efficacy of antibiotic prophylaxis for GI and GU procedures and guidelines of GI and GU societies are discordant. Antibiotic prophylaxis may be unnecessary for less invasive GI or GU endoscopic procedures, but it may be beneficial for prevention of PJI at least for certain high-risk patients who undergo more invasive procedures.110

Future Directions An attractive strategy for preventing PJI is the design of socalled smart implants, with coating surfaces that would improve osseointegration and reduce bacterial attachment and biofilm formation. Proposed methods include coating with antibiotics (such as vancomycin)111 or nonantibiotic antibacterial materials (silver, nitrite oxide, and chitosan),112

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modification of the implant surface into a more hydrophilic surface to make it less susceptible to bacterial adhesion,113 enhancing osseointegration, and combining methods.114 Concerns regarding antibiotic resistance exist with the use of antibiotic-coating surfaces. Silver is an efficient bactericidal agent, but there might be some concerns with its use, such as wear issues, toxicity for human cells, and thrombogenicity.112 Anti-adhesion coatings are aimed to prevent the initial phase of biofilm formation. Several techniques have been proposed, including the attachment of hydrophobic molecules, changing surface roughness, and charges.113,115 Despite these advances, substantial research is warranted before these methods can be clinically applied. Another interesting field of recent research over the past two decades has been searching for vaccines against S. aureus. Two main targets for such vaccines are capsular polysaccharides and microbial surface components recognizing adhesive matrix molecules proteins that facilitate binding of S. aureus to a variety of extracellular matrix proteins.116 However, clinical data confirming long-term efficacy of these vaccines are lacking and two large-scale phase 3 studies on patients undergoing cardiothoracic surgery117 and patients under hemodialysis118 have failed to provide prolonged protection.

Conclusion Prevention of PJI requires implementation of strategies that include numerous aspects of preoperative, perioperative, and postoperative care of patients. Some strategies such as elimination of modifiable risk factors (such as uncontrolled hyperglycemia, smoking, malnutrition, and substance abuse), use of perioperative antibiotic prophylaxis, and execution of surgical safety checklist have successfully reduced the incidence of SSI and PJI. These strategies should be broadly adopted. On the contrary, available evidence for other strategies shows some benefit, though more work is required for their optimization. Examples are methods for skin preparation, nasal decolonization, and surgical wound irrigation and closure. Further research is required to reinforce our armamentarium against infection with optimization of currently practiced methods and introduction of novel effective approaches.

References 1 Furnary AP, Wu Y. Eliminating the diabetic disadvantage: the

Portland Diabetic Project. Semin Thorac Cardiovasc Surg 2006; 18(4):302–308 2 Marchant MH Jr, Viens NA, Cook C, Vail TP, Bolognesi MP. The impact of glycemic control and diabetes mellitus on perioperative outcomes after total joint arthroplasty. J Bone Joint Surg Am 2009;91(7):1621–1629 3 Mraovic B, Suh D, Jacovides C, Parvizi J. Perioperative hyperglycemia and postoperative infection after lower limb arthroplasty. J Diabetes Sci Tech 2011;5(2):412–418 4 Umpierrez GE, Hellman R, Korytkowski MT, et al; Endocrine Society. Management of hyperglycemia in hospitalized patients in non-critical care setting: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 2012; 97(1):16–38 The Journal of Knee Surgery

Vol. 27

No. 4/2014

255

Downloaded by: WEST VIRGINIA UNIVERSITY. Copyrighted material.

Prevention of Periprosthetic Joint Infection

Prevention of Periprosthetic Joint Infection

Alijanipour et al.

5 Peersman G, Laskin R, Davis J, Peterson M. Infection in total knee

28 Patel VP, Walsh M, Sehgal B, Preston C, DeWal H, Di Cesare PE.

replacement: a retrospective review of 6489 total knee replacements. Clin Orthop Relat Res 2001;(392):15–23 Lai K, Bohm ER, Burnell C, Hedden DR. Presence of medical comorbidities in patients with infected primary hip or knee arthroplasties. J Arthroplasty 2007;22(5):651–656 Meding JB, Reddleman K, Keating ME, et al. Total knee replacement in patients with diabetes mellitus. Clin Orthop Relat Res 2003;(416):208–216 Pozzilli P, Leslie RD. Infections and diabetes: mechanisms and prospects for prevention. Diabet Med 1994;11(10):935–941 Papagelopoulos PJ, Idusuyi OB, Wallrichs SL, Morrey BF. Long term outcome and survivorship analysis of primary total knee arthroplasty in patients with diabetes mellitus. Clin Orthop Relat Res 1996;(330):124–132 Yang K, Yeo SJ, Lee BP, Lo NN. Total knee arthroplasty in diabetic patients: a study of 109 consecutive cases. J Arthroplasty 2001; 16(1):102–106 Moeckel B, Huo MH, Salvati EA, Pellicci PM. Total hip arthroplasty in patients with diabetes mellitus. J Arthroplasty 1993;8(3): 279–284 Jämsen E, Nevalainen P, Kalliovalkama J, Moilanen T. Preoperative hyperglycemia predicts infected total knee replacement. Eur J Intern Med 2010;21(3):196–201 Soohoo NF, Farng E, Lieberman JR, Chambers L, Zingmond DS. Factors that predict short-term complication rates after total hip arthroplasty. Clin Orthop Relat Res 2010;468(9):2363–2371 American Diabetes Association. Standards of medical care in diabetes—2008. Diabetes Care 2008;31(Suppl 1):S12–S54 Del Savio GC, Zelicof SB, Wexler LM, et al. Preoperative nutritional status and outcome of elective total hip replacement. Clin Orthop Relat Res 1996;(326):153–161 Lavernia CJ, Sierra RJ, Baerga L. Nutritional parameters and short term outcome in arthroplasty. J Am Coll Nutr 1999;18(3): 274–278 Greene KA, Wilde AH, Stulberg BN. Preoperative nutritional status of total joint patients. Relationship to postoperative wound complications. J Arthroplasty 1991;6(4):321–325 Gherini S, Vaughn BK, Lombardi AV Jr, Mallory TH. Delayed wound healing and nutritional deficiencies after total hip arthroplasty. Clin Orthop Relat Res 1993;(293):188–195 Marín LA, Salido JA, López A, Silva A. Preoperative nutritional evaluation as a prognostic tool for wound healing. Acta Orthop Scand 2002;73(1):2–5 Nawabi DH, Chin KF, Keen RW, Haddad FS. Vitamin D deficiency in patients with osteoarthritis undergoing total hip replacement: a cause for concern? J Bone Joint Surg Br 2010;92(4):496–499 Pulido L, Ghanem E, Joshi A, Purtill JJ, Parvizi J. Periprosthetic joint infection: the incidence, timing, and predisposing factors. Clin Orthop Relat Res 2008;466(7):1710–1715 Dowsey MM, Choong PFM. Obesity is a major risk factor for prosthetic infection after primary hip arthroplasty. Clin Orthop Relat Res 2008;466(1):153–158 Lübbeke A, Stern R, Garavaglia G, Zurcher L, Hoffmeyer P. Differences in outcomes of obese women and men undergoing primary total hip arthroplasty. Arthritis Rheum 2007;57(2):327–334 Namba RS, Paxton L, Fithian DC, Stone ML. Obesity and perioperative morbidity in total hip and total knee arthroplasty patients. J Arthroplasty 2005;20(7, Suppl 3):46–50 Gandhi R, Razak F, Davey JR, Mahomed NN. Metabolic syndrome and the functional outcomes of hip and knee arthroplasty. J Rheumatol 2010;37(9):1917–1922 Winiarsky R, Barth P, Lotke P. Total knee arthroplasty in morbidly obese patients. J Bone Joint Surg Am 1998;80(12): 1770–1774 Hopf HW, Hunt TK, West JM, et al. Wound tissue oxygen tension predicts the risk of wound infection in surgical patients. Arch Surg 1997;132(9):997–1004, discussion 1005

Factors associated with prolonged wound drainage after primary total hip and knee arthroplasty. J Bone Joint Surg Am 2007;89(1): 33–38 Parvizi J, Trousdale RT, Sarr MG. Total joint arthroplasty in patients surgically treated for morbid obesity. J Arthroplasty 2000;15(8):1003–1008 Freeman JT, Anderson DJ, Hartwig MG, Sexton DJ. Surgical site infections following bariatric surgery in community hospitals: a weighty concern? Obes Surg 2011;21(7):836–840 Jorgensen LN, Kallehave F, Christensen E, Siana JE, Gottrup F. Less collagen production in smokers. Surgery 1998;123(4):450–455 Sadr Azodi O, Bellocco R, Eriksson K, Adami J. The impact of tobacco use and body mass index on the length of stay in hospital and the risk of post-operative complications among patients undergoing total hip replacement. J Bone Joint Surg Br 2006; 88(10):1316–1320 Singh JA. Smoking and outcomes after knee and hip arthroplasty: a systematic review. J Rheumatol 2011;38(9):1824–1834 Møller AM, Villebro N, Pedersen T, Tønnesen H. Effect of preoperative smoking intervention on postoperative complications: a randomised clinical trial. Lancet 2002;359(9301):114–117 Mills E, Eyawo O, Lockhart I, Kelly S, Wu P, Ebbert JO. Smoking cessation reduces postoperative complications: a systematic review and meta-analysis. Am J Med 2011;124(2):144–154, e8 Bradley KA, Rubinsky AD, Sun H, et al. Alcohol screening and risk of postoperative complications in male VA patients undergoing major non-cardiac surgery. J Gen Intern Med 2011;26(2): 162–169 Harris AHS, Reeder R, Ellerbe L, Bradley KA, Rubinsky AD, Giori NJ. Preoperative alcohol screening scores: association with complications in men undergoing total joint arthroplasty. J Bone Joint Surg Am 2011;93(4):321–327 Tønnesen H, Petersen KR, Højgaard L, et al. Postoperative morbidity among symptom-free alcohol misusers. Lancet 1992; 340(8815):334–337 Tonnesen H, Rosenberg J, Nielsen HJ, et al. Effect of preoperative abstinence on poor postoperative outcome in alcohol misusers: randomised controlled trial. BMJ 1999;318(7194):1311–1316 Habermann B, Eberhardt C, Kurth AA. Total joint replacement in HIV positive patients. J Infect 2008;57(1):41–46 Sunday JM, Guille JT, Torg JS. Complications of joint arthroplasty in patients with end-stage renal disease on hemodialysis. Clin Orthop Relat Res 2002;(397):350–355 Lieberman JR, Fuchs MD, Haas SB, et al. Hip arthroplasty in patients with chronic renal failure. J Arthroplasty 1995;10(2): 191–195 Pour AE, Matar WY, Jafari SM, Purtill JJ, Austin MS, Parvizi J. Total joint arthroplasty in patients with hepatitis C. J Bone Joint Surg Am 2011;93(15):1448–1454 Hsieh PH, Chen LH, Lee MS, Chen CH, Yang WE, Shih CH. Hip arthroplasty in patients with cirrhosis of the liver. J Bone Joint Surg Br 2003;85(6):818–821 Luck JV Jr, Logan LR, Benson DR, Glasser DB. Human immunodeficiency virus infection: complications and outcome of orthopaedic surgery. J Am Acad Orthop Surg 1996;4(6):297–304 Vergidis P, Lesnick TG, Kremers WK, Razonable RR. Prosthetic joint infection in solid organ transplant recipients: a retrospective case-control study. Transpl Infect Dis 2012;14(4):380–386 Schrama JC, Espehaug B, Hallan G, et al. Risk of revision for infection in primary total hip and knee arthroplasty in patients with rheumatoid arthritis compared with osteoarthritis: a prospective, population-based study on 108,786 hip and knee joint arthroplasties from the Norwegian Arthroplasty Register. Arthritis Care Res (Hoboken) 2010;62(4):473–479 Sakalkale DP, Hozack WJ, Rothman RH. Total hip arthroplasty in patients on long-term renal dialysis. J Arthroplasty 1999;14(5): 571–575

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49 Tannenbaum DA, Matthews LS, Grady-Benson JC. Infection

65 Hooper GJ, Rothwell AG, Frampton C, Wyatt MC. Does the use of

around joint replacements in patients who have a renal or liver transplantation. J Bone Joint Surg Am 1997;79(1):36–43 Parvizi J, Zmistowski B, Berbari EF, et al. New definition for periprosthetic joint infection: from the Workgroup of the Musculoskeletal Infection Society. Clin Orthop Relat Res 2011; 469(11):2992–2994 Bombardier C, Hazlewood GS, Akhavan P, et al; Canadian Rheumatology Association. Canadian Rheumatology Association recommendations for the pharmacological management of rheumatoid arthritis with traditional and biologic disease-modifying antirheumatic drugs: part II safety. J Rheumatol 2012;39(8): 1583–1602 Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis 2008;197(9): 1226–1234 Perl TM, Golub JE. New approaches to reduce Staphylococcus aureus nosocomial infection rates: treating S. aureus nasal carriage. Ann Pharmacother 1998;32(1):S7–S16 Schweizer M, Perencevich E, McDanel J, et al. Effectiveness of a bundled intervention of decolonization and prophylaxis to decrease Gram positive surgical site infections after cardiac or orthopedic surgery: systematic review and meta-analysis. BMJ 2013;346:f2743 Van Rijen M, Bonten M, Wenzel R, et al. Mupirocin ointment for preventing Staphylococcus aureus infections in nasal carriers. In: The Cochrane Library. Available at: http://onlinelibrary.wiley. com/doi/10.1002/14651858.CD006216.pub2/abstract. Accessed March 8, 2012 Young LS, Winston LG. Preoperative use of mupirocin for the prevention of healthcare-associated Staphylococcus aureus infections: a cost-effectiveness analysis. Infect Control Hosp Epidemiol 2006;27(12):1304–1312 Perl TM, Cullen JJ, Wenzel RP, et al; Mupirocin And The Risk Of Staphylococcus Aureus Study Team. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 2002;346(24):1871–1877 Courville XF, Tomek IM, Kirkland KB, Birhle M, Kantor SR, Finlayson SRG. Cost-effectiveness of preoperative nasal mupirocin treatment in preventing surgical site infection in patients undergoing total hip and knee arthroplasty: a cost-effectiveness analysis. Infect Control Hosp Epidemiol 2012;33(2):152–159 Screening for Methicillin-Resistant Staphylococcus Aureus (MRSA) Executive Summary. Available at: http://effectivehealthcare.ahrq.gov/ehc/products/228/1551/MRSA-screening-executive-130617.pdf. Accessed January 28, 2014 Economedes DM, Deirmengian GK, Deirmengian CA. Staphylococcus aureus colonization among arthroplasty patients previously treated by a decolonization protocol: a pilot study. Clin Orthop Relat Res 2013;471(10):3128–3132 Lidwell OM, Lowbury EJ, Whyte W, Blowers R, Stanley SJ, Lowe D. Airborne contamination of wounds in joint replacement operations: the relationship to sepsis rates. J Hosp Infect 1983;4(2): 111–131 Stocks GW, Self SD, Thompson B, Adame XA, O’Connor DP. Predicting bacterial populations based on airborne particulates: a study performed in nonlaminar flow operating rooms during joint arthroplasty surgery. Am J Infect Control 2010;38(3): 199–204 Brandt C, Hott U, Sohr D, Daschner F, Gastmeier P, Rüden H. Operating room ventilation with laminar airflow shows no protective effect on the surgical site infection rate in orthopedic and abdominal surgery. Ann Surg 2008;248(5):695–700 Breier A-C, Brandt C, Sohr D, Geffers C, Gastmeier P. Laminar airflow ceiling size: no impact on infection rates following hip and knee prosthesis. Infect Control Hosp Epidemiol 2011;32(11): 1097–1102

laminar flow and space suits reduce early deep infection after total hip and knee replacement?: the ten-year results of the New Zealand Joint Registry J Bone Joint Surg Br 2011;93(1):85–90 Miner AL, Losina E, Katz JN, Fossel AH, Platt R. Deep infection after total knee replacement: impact of laminar airflow systems and body exhaust suits in the modern operating room. Infect Control Hosp Epidemiol 2007;28(2):222–226 Evans RP. Current concepts for clean air and total joint arthroplasty: laminar airflow and ultraviolet radiation: a systematic review. Clin Orthop Relat Res 2011;469(4):945–953 Panahi P, Stroh M, Casper DS, Parvizi J, Austin MS. Operating room traffic is a major concern during total joint arthroplasty. Clin Orthop Relat Res 2012;470(10):2690–2694 de Vries EN, Prins HA, Crolla RMPH, et al; SURPASS Collaborative Group. Effect of a comprehensive surgical safety system on patient outcomes. N Engl J Med 2010;363(20):1928–1937 Haynes AB, Weiser TG, Berry WR, et al; Safe Surgery Saves Lives Study Group. A surgical safety checklist to reduce morbidity and mortality in a global population. N Engl J Med 2009;360(5): 491–499 Rosenberg AD, Wambold D, Kraemer L, et al. Ensuring appropriate timing of antimicrobial prophylaxis. J Bone Joint Surg Am 2008;90(2):226–232 Melling AC, Ali B, Scott EM, Leaper DJ. Effects of preoperative warming on the incidence of wound infection after clean surgery: a randomised controlled trial. Lancet 2001;358(9285):876–880 Sessler DI, Olmsted RN, Kuelpmann R. Forced-air warming does not worsen air quality in laminar flow operating rooms. Anesth Analg 2011;113(6):1416–1421 Legg AJ, Hamer AJ. Forced-air patient warming blankets disrupt unidirectional airflow. Bone Joint J 2013;95-B(3):407–410 Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR; Hospital Infection Control Practices Advisory Committee. Guideline for prevention of surgical site infection, 1999. Infect Control Hosp Epidemiol 1999;20(4):250–278, quiz 279–280 Tanner J, Norrie P, Melen K. Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev 2011;(11): CD004122 Darouiche RO, Wall MJ Jr, Itani KMF, et al. Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. N Engl J Med 2010;362(1):18–26 Swenson BR, Hedrick TL, Metzger R, Bonatti H, Pruett TL, Sawyer RG. Effects of preoperative skin preparation on postoperative wound infection rates: a prospective study of 3 skin preparation protocols. Infect Control Hosp Epidemiol 2009;30(10):964–971 Blom A, Estela C, Bowker K, MacGowan A, Hardy JR. The passage of bacteria through surgical drapes. Ann R Coll Surg Engl 2000; 82(6):405–407 Webster J, Alghamdi A. Use of plastic adhesive drapes during surgery for preventing surgical site infection. Cochrane Database Syst Rev 2013;1:CD006353 Alexander JW, Aerni S, Plettner JP. Development of a safe and effective one-minute preoperative skin preparation. Arch Surg 1985;120(12):1357–1361 Jacobson C, Osmon DR, Hanssen A, et al. Prevention of wound contamination using DuraPrep solution plus Ioban 2 drapes. Clin Orthop Relat Res 2005;439(439):32–37 Anglen JO, Gainor BJ, Simpson WA, Christensen G. The use of detergent irrigation for musculoskeletal wounds. Int Orthop 2003;27(1):40–46 Cheng M-T, Chang M-C, Wang S-T, Yu W-K, Liu C-L, Chen T-H. Efficacy of dilute betadine solution irrigation in the prevention of postoperative infection of spinal surgery. Spine 2005;30(15): 1689–1693 Schein M, Gecelter G, Freinkel W, Gerding H, Becker PJ. Peritoneal lavage in abdominal sepsis. A controlled clinical study. Arch Surg 1990;125(9):1132–1135

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Prevention of Periprosthetic Joint Infection

Alijanipour et al.

86 Conroy BP, Anglen JO, Simpson WA, et al. Comparison of castile

101 Koval KJ, Rosenberg AD, Zuckerman JD, et al. Does blood transfu-

soap, benzalkonium chloride, and bacitracin as irrigation solutions for complex contaminated orthopaedic wounds. J Orthop Trauma 1999;13(5):332–337 Niki Y, Matsumoto H, Otani T, Tomatsu T, Toyama Y. How much sterile saline should be used for efficient lavage during total knee arthroplasty? Effects of pulse lavage irrigation on removal of bone and cement debris. J Arthroplasty 2007;22(1):95–99 Seeger JB, Jaeger S, Bitsch RG, Mohr G, Röhner E, Clarius M. The effect of bone lavage on femoral cement penetration and interface temperature during Oxford unicompartmental knee arthroplasty with cement. J Bone Joint Surg Am 2013;95(1):48–53 Kalteis T, Pförringer D, Herold T, Handel M, Renkawitz T, Plitz W. An experimental comparison of different devices for pulsatile high-pressure lavage and their relevance to cement intrusion into cancellous bone. Arch Orthop Trauma Surg 2007;127(10): 873–877 Hassinger SM, Harding G, Wongworawat MD. High-pressure pulsatile lavage propagates bacteria into soft tissue. Clin Orthop Relat Res 2005;439(439):27–31 Polzin B, Ellis T, Dirschl DR. Effects of varying pulsatile lavage pressure on cancellous bone structure and fracture healing. J Orthop Trauma 2006;20(4):261–266 Smith TO, Sexton D, Mann C, Donell S. Sutures versus staples for skin closure in orthopaedic surgery: meta-analysis. BMJ 2010; 340:c1199 AlBuhairan B, Hind D, Hutchinson A. Antibiotic prophylaxis for wound infections in total joint arthroplasty: a systematic review. J Bone Joint Surg Br 2008;90(7):915–919 Peel TN, Cheng AC, Buising KL, Choong PFM. Microbiological aetiology, epidemiology, and clinical profile of prosthetic joint infections: are current antibiotic prophylaxis guidelines effective? Antimicrob Agents Chemother 2012;56(5):2386–2391 van Kasteren MEE, Manniën J, Ott A, Kullberg B-J, de Boer AS, Gyssens IC. Antibiotic prophylaxis and the risk of surgical site infections following total hip arthroplasty: timely administration is the most important factor. Clin Infect Dis 2007;44(7): 921–927 Parvizi J, Saleh KJ, Ragland PS, Pour AE, Mont MA. Efficacy of antibiotic-impregnated cement in total hip replacement. Acta Orthop 2008;79(3):335–341 Engesaeter LB, Lie SA, Espehaug B, Furnes O, Vollset SE, Havelin LI. Antibiotic prophylaxis in total hip arthroplasty: effects of antibiotic prophylaxis systemically and in bone cement on the revision rate of 22,170 primary hip replacements followed 0-14 years in the Norwegian Arthroplasty Register. Acta Orthop Scand 2003; 74(6):644–651 Bohm E, Zhu N, Gu J, et al. Does adding antibiotics to cement reduce the need for early revision in total knee arthroplasty? Clin Orthop Relat Res 2014;472(1):162–168 Namba RS, Inacio MCS, Paxton EW. Risk factors associated with deep surgical site infections after primary total knee arthroplasty: an analysis of 56,216 knees. J Bone Joint Surg Am 2013; 95(9):775–782 Innerhofer P, Klingler A, Klimmer C, Fries D, Nussbaumer W. Risk for postoperative infection after transfusion of white blood cellfiltered allogeneic or autologous blood components in orthopedic patients undergoing primary arthroplasty. Transfusion 2005; 45(1):103–110

sion increase the risk of infection after hip fracture? J Orthop Trauma 1997;11(4):260–265, discussion 265–266 Spahn DR. Anemia and patient blood management in hip and knee surgery: a systematic review of the literature. Anesthesiology 2010;113(2):482–495 Alshryda S, Sarda P, Sukeik M, Nargol A, Blenkinsopp J, Mason JM. Tranexamic acid in total knee replacement: a systematic review and meta-analysis. J Bone Joint Surg Br 2011;93(12):1577–1585 Yang Z-G, Chen W-P, Wu L-D. Effectiveness and safety of tranexamic acid in reducing blood loss in total knee arthroplasty: a meta-analysis. J Bone Joint Surg Am 2012;94(13):1153–1159 American Academy of Orthopedic Surgeons. AAOS Clinical Practice Guideline: Prevention of Orthopaedic Implant Infection in Patients Undergoing Dental Procedures. Available at: http:// www.aaos.org/research/guidelines/PUDP/PUDP_guideline.pdf. Accessed January 28, 2014 Takai S, Kuriyama T, Yanagisawa M, Nakagawa K, Karasawa T. Incidence and bacteriology of bacteremia associated with various oral and maxillofacial surgical procedures. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;99(3):292–298 Heimdahl A, Hall G, Hedberg M, et al. Detection and quantitation by lysis-filtration of bacteremia after different oral surgical procedures. J Clin Microbiol 1990;28(10):2205–2209 Lockhart PB, Loven B, Brennan MT, Fox PC. The evidence base for the efficacy of antibiotic prophylaxis in dental practice. J Am Dent Assoc 2007;138(4):458–474, quiz 534–535, 437 Tomás I, Diz P, Tobías A, Scully C, Donos N. Periodontal health status and bacteraemia from daily oral activities: systematic review/meta-analysis. J Clin Periodontol 2012;39(3):213–228 Parvizi J, Gehrke T, Chen AF. Proceedings of the International Consensus on Periprosthetic Joint Infection. Bone Joint J 2013;95B(11):1450–1452 Antoci V Jr, Adams CS, Parvizi J, et al. The inhibition of Staphylococcus epidermidis biofilm formation by vancomycin-modified titanium alloy and implications for the treatment of periprosthetic infection. Biomaterials 2008;29(35):4684–4690 Chen M, Yu Q, Sun H. Novel strategies for the prevention and treatment of biofilm related infections. Int J Mol Sci 2013;14(9): 18488–18501 Tang H, Cao T, Liang X, et al. Influence of silicone surface roughness and hydrophobicity on adhesion and colonization of Staphylococcus epidermidis. J Biomed Mater Res A 2009;88(2):454–463 Arciola CR, Montanaro L, Costerton JW. New trends in diagnosis and control strategies for implant infections. Int J Artif Organs 2011;34(9):727–736 Truong VK, Lapovok R, Estrin YS, et al. The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 2010;31(13):3674–3683 Montanaro L, Speziale P, Campoccia D, et al. Scenery of Staphylococcus implant infections in orthopedics. Future Microbiol 2011; 6(11):1329–1349 Harro C, Betts R, Orenstein W, et al. Safety and immunogenicity of a novel Staphylococcus aureus vaccine: results from the first study of the vaccine dose range in humans. Clin Vaccine Immunol 2010; 17(12):1868–1874 Shinefield H, Black S, Fattom A, et al. Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med 2002;346(7):491–496

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