periprosthetic shoulder infections

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Current Concepts Review Diagnosis and Management of Periprosthetic Shoulder Infections William R. Mook, MD, and Grant E. Garrigues, MD Investigation performed at the Department of Orthopaedic Surgery, Duke University Medical Center, Durham, North Carolina ä The unique bacterial flora of the shoulder present diagnostic and treatment challenges that are distinct from those seen with failed hip and knee arthroplasties. ä The presentation, diagnosis, and management of suppurative periprosthetic joint infections of the shoulder are similar to those of the hip and the knee. ä Failed arthroplasties with positive cultures (FAPCs) are poorly performing shoulder reconstructions associated with low-virulence microorganisms that do not evoke a suppurative inflammatory response. Propionibacterium acnes is the predominant bacterium isolated from these cases. ä With improved surgeon awareness and the addition of longer tissue-culture incubation times, detection of FAPCs has become more common. However, management is hampered by the lack of reliable, timely tests that can determine the presence of less virulent organisms in the preoperative or intraoperative settings. ä The implications of positive culture results in FAPCs are unclear. Key test characteristics such as the false-positive rate and the prevalence of positive cultures in well-performing shoulders are unknown as there is no useful confirmatory test to validate the culture data and no reliable way to detect the presence of less virulent micro- organisms without reoperation. ä Soft-tissue and osseous deficits are frequently encountered when revising previously infected shoulders. The rate of complications in these scenarios is high, and the outcomes are the least favorable compared with revisions for any other indication. ä The development of a consensus definition of a periprosthetic shoulder infection is critical to future investigations of these devastating complications. Over 45,000 shoulder arthroplasties are performed each year in the United States, and the number is increasing rapidly 1 . Re- visions of shoulder arthroplasties because of failure or infection are also expected to rise 2 . According to the traditional definition of periprosthetic joint infections 3-6 , periprosthetic shoulder infec- tions after primary arthroplasties are rare, with a prevalence as low Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article. Peer Review: This article was reviewed by the Editor-in-Chief and one Deputy Editor, and it underwent blinded review by two or more outside experts. It was also reviewed by an expert in methodology and statistics. The Deputy Editor reviewed each revision of the article, and it underwent a final review by the Editor-in-Chief prior to publication. Final corrections and clarifications occurred during one or more exchanges between the author(s) and copyeditors. 956 COPYRIGHT Ó 2014 BY THE J OURNAL OF BONE AND J OINT SURGERY,I NCORPORATED J Bone Joint Surg Am. 2014;96:956-65 d http://dx.doi.org/10.2106/JBJS.M.00402

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Periprosthetic Shoulder Infections

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Page 1: Periprosthetic Shoulder Infections

Current Concepts Review

Diagnosis and Management ofPeriprosthetic Shoulder Infections

William R. Mook, MD, and Grant E. Garrigues, MD

Investigation performed at the Department of Orthopaedic Surgery, Duke University Medical Center, Durham, North Carolina

� The unique bacterial flora of the shoulder present diagnostic and treatment challenges that are distinct from thoseseen with failed hip and knee arthroplasties.

� The presentation, diagnosis, and management of suppurative periprosthetic joint infections of the shoulder aresimilar to those of the hip and the knee.

� Failed arthroplasties with positive cultures (FAPCs) are poorly performing shoulder reconstructions associatedwith low-virulence microorganisms that do not evoke a suppurative inflammatory response. Propionibacteriumacnes is the predominant bacterium isolated from these cases.

� With improved surgeon awareness and the addition of longer tissue-culture incubation times, detection of FAPCshas become more common. However, management is hampered by the lack of reliable, timely tests that candetermine the presence of less virulent organisms in the preoperative or intraoperative settings.

� The implications of positive culture results in FAPCs are unclear. Key test characteristics such as the false-positiverate and the prevalence of positive cultures in well-performing shoulders are unknown as there is no usefulconfirmatory test to validate the culture data and no reliable way to detect the presence of less virulent micro-organisms without reoperation.

� Soft-tissue and osseous deficits are frequently encountered when revising previously infected shoulders. The rateof complications in these scenarios is high, and the outcomes are the least favorable compared with revisions forany other indication.

� The development of a consensus definition of a periprosthetic shoulder infection is critical to future investigationsof these devastating complications.

Over 45,000 shoulder arthroplasties are performed each yearin the United States, and the number is increasing rapidly1. Re-visions of shoulder arthroplasties because of failure or infection

are also expected to rise2. According to the traditional definition ofperiprosthetic joint infections3-6, periprosthetic shoulder infec-tions after primary arthroplasties are rare, with a prevalence as low

Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of anyaspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, withany entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had anyother relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. Thecomplete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

Peer Review: This article was reviewed by the Editor-in-Chief and one Deputy Editor, and it underwent blinded review by two or more outside experts. It was also reviewedby an expert in methodology and statistics. The Deputy Editor reviewed each revision of the article, and it underwent a final review by the Editor-in-Chief prior to publication.Final corrections and clarifications occurred during one or more exchanges between the author(s) and copyeditors.

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J Bone Joint Surg Am. 2014;96:956-65 d http://dx.doi.org/10.2106/JBJS.M.00402

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as 0.7%7 for primary arthroplasties, but as high as 15.4%8 for re-visions. However, these estimates precede the development of ourcurrent culture techniques and understanding of less virulent mi-croorganisms, particularly Propionibacterium acnes and coagulase-negative Staphylococcus, in failed shoulder arthroplasties.

The characteristics of most periprosthetic joint infectionsof the hip and knee are unlike those of the shoulder. The pre-sentation, natural history, and prognoses of periprosthetic hipand knee infections have been more extensively studied be-cause of their increased prevalence compared with peri-prosthetic shoulder infections9,10. Unfortunately, the principlesfor the evaluation and management of periprosthetic hip andknee infections are not generally applicable to the shoulder.

The purpose of this review is to synthesize the currentliterature as it pertains to the diagnosis and treatment of peri-prosthetic shoulder infection, indicate where distinctions be-tween periprosthetic infections of other joints exist and why,and provide evidence-based recommendations to help guidetheir management and future investigations (Table I)11.

Clinical EvaluationA high index of suspicion for indolent infection must bemaintained when any patient with a poorly performingshoulder replacement is evaluated. The surgeon should elicit acomprehensive clinical history and follow it with a focusedexamination of the shoulder girdle as the first step in evaluatinga patient with dissatisfaction following shoulder arthroplasty.Risk factors for periprosthetic hip and knee infections, in-cluding obesity12-15, poorly controlled diabetes mellitus12,16, in-flammatory skin conditions17, chronic immunosuppression18,

malignancy19, and inflammatory arthropathy20, should be noted.While these patient-related risk factors for infection followingshoulder arthroplasty have been evaluated, only postoperativehematoma21, arthroplasty after trauma22, younger age23, and malesex23,24 have been identified as significant risk factors for peri-prosthetic shoulder infection.

The clinician also should elicit any potential sources ofhematogenous inoculation of the prosthesis, such as recent urinarytract infection, oral abscess, or pneumonia. Any issues present withprior shoulder operations, such as erythema, drainage, swelling,warmth, fever, chills, and treatment with antibiotics, should besought out and should raise the surgeon’s level of suspicion of aninfection caused by a more virulent organism.

In the Mayo Clinic experience with periprosthetic shoul-der infection, shoulder pain was the most common complaint(86%), followed by a draining sinus (44%), stiffness (35%), er-ythema (35%), effusion (32%), fever (21%), night sweats (9%),and chills (9%)25. They also noted that since 2000, P. acnes wasidentified at revision as frequently as Staphylococcus species22,23.Unlike virulent staphylococcal infections, with periprostheticP. acnes infections, purulence is rarely observed24,26,27. (A detaileddiscussion regarding the unique microbiologic profile of theshoulder and the challenges to arriving at a universally accepteddefinition of a periprosthetic shoulder infection is available inthe Appendix).

ImagingPatients should be evaluated with high-quality radiographs,especially anteroposterior and axillary lateral projections, torule out causes of shoulder pain and dysfunction that can

TABLE I Grades of Recommendation for the Diagnosis and Management of Periprosthetic Shoulder Infections

Recommendation* Grade†

DiagnosisPreoperative serum ESR and CRP values, as well as joint aspirations for the evaluation of synovial fluid leukocytecounts and bacterial culture, lack the sensitivity and specificity necessary to accurately identify most periprostheticshoulder infections, especially those caused by P. acnes and coagulase-negative Staphylococcus.

C

Cultures of periprosthetic tissue and synovial fluid samples obtained at the time of revision are currently the mostsensitive and specific tests in the diagnosis of periprosthetic shoulder infections.

C

Both aerobic and anaerobic cultures should be held for at least fourteen days of incubation. C

ManagementSurgical outcomes are superior to those of medical management. Antibiotic suppression alone is reserved for patientsunwilling or medically unable to undergo a repeat operation.

C

Resection arthroplasty or the insertion of an articulating antibiotic spacer as definitive treatment are options associatedwith relatively low infection recurrence rates and may be suitable for patients with low functional demands and/or theinability to undergo additional procedures due to medical comorbidities.

C

In higher functional demand patients with suppurative infections, debridement, targeted antibiosis, and stagedreimplantation are recommended.

B

In the setting of FAPC with less virulent microorganisms such as P. acnes and coagulase-negative Staphylococcus,debridement with implant retention as well as one and two-stage revisions are treatment options.

I

*ESR = erythrocyte sedimentation rate, CRP = C-reactive protein, and FAPC = failed arthroplasty with positive cultures. †A = consensus agreementor good evidence (Level-I studies with consistent findings) for or against the recommendation, B = fair evidence (Level-II or III studies withconsistent findings) for or against recommending intervention, C = conflicting or poor-quality evidence (Level-IV of V studies) not allowing arecommendation for or against intervention, and I = there is insufficient evidence to make a recommendation11.

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mimic, or coexist with, periprosthetic shoulder infection (Fig.1). As in periprosthetic hip and knee infections, there are ra-diographic signs28-30 that may support the diagnosis of peri-prosthetic shoulder infection (Table II), although they are

similarly nonspecific24,25. It is also critically important to notesubtle changes in serial radiographs over time (Figs. 2-A and2-B). Pottinger et al. found that progressive humeral osteolysisimparted a tenfold increase in the prognostic risk of a P. acnesinfection24.

Computed tomography (CT) and magnetic resonanceimaging (MRI) with metal artifact reduction protocols may behelpful in narrowing the differential diagnosis and for preoper-ative planning, but they rarely change the management plan whenthe diagnosis of infection is finally made. If the diagnosis of peri-prosthetic shoulder infection is confirmed, a CT scan may bemore useful after removal of the components, debridement, andantibiotic spacer placement to determine the bone stock presentfor revision arthroplasty. Similar to the evaluation of failing lower-extremity prostheses31-35, radionucleotide scans have limited utilityin isolation in the evaluation of suspected periprosthetic shoulderinfection. Evidence-based recommendations regarding theirroutine use in the evaluation of a possible periprosthetic shoulderinfection cannot be made because of a dearth of high-level clinicalevidence.

Fig. 1

Causes of shoulder pain and dysfunction characteristic of implant type (humeral head hemiarthroplasty, total shoulder arthroplasty [TSA], or reverse total

shoulder arthroplasty) that can mimic, or coexist with, periprosthetic joint infection.

TABLE II Radiographic Signs Consistent with PeriprostheticInfection*

Effusion

Endosteal scalloping

Generalized bone resorption

Periosteal reaction

Periprosthetic radiolucent lines

Radiolucent osseous sinus

Scattered osteolysis

*Based on the studies by Pottinger et al.24, Sperlinget al.25, Tiggeset al.28, Bauer et al.29, and Zimmerli et al.30.

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Serologic TestsAlthough the measurements of the erythrocyte sedimentationrate (ESR) and C-reactive protein (CRP) level are excellentscreening tests in the evaluation of possible periprosthetic jointinfections of the hip and knee6,29,36-39, the sensitivity and speci-ficity of these screening tools have not been demonstrated to besufficiently high enough to allow for periprosthetic shoulderinfection to be ruled in or out, especially with an indolent in-fection such as those caused by P. acnes or coagulase-negativeStaphylococcus26,27,40-45.

In the evaluation of periprosthetic joint infection of thehip and knee, these tests have a high negative predictive value,indicating that when both the ESR and CRP results are normal,infection is unlikely3. In contrast, a recent series of seventy-fiveshoulders with positive intraoperative cultures during revisionarthroplasty revealed that only 25% (four) of sixteen patientswho had testing of the CRP level had a positive result and only14% (six) of forty-two who had testing of the ESR had a pos-itive result44. In a series of patients in whom P. acnes shoulderinfections were identified by Millet et al., only 10% (one) of tenpatients had an elevation of both inflammatory markers27. Inthe largest series to evaluate factors prognostic for obtainingpositive bacterial cultures in revision shoulder surgery, neitherserologic test was significantly associated with an increasedlikelihood of a positive culture44. Therefore, normal laboratorypreoperative inflammatory markers do not rule out the pres-ence of a periprosthetic shoulder infection, and additionalworkup for infection may be indicated.

There are a number of inflammatory conditions that canalso lead to the elevation of these serum markers. Both inflam-matory markers rise rapidly following uncomplicated surgeryand return to normal levels at variable rates46, with CRP tendingto normalize more quickly than ESR47. In general, CRP levelspeak two to three days after surgery and return to normal by threeto six weeks. Changes in ESR values following uncomplicated

surgery are less predictable, but generally peak five days aftersurgery and normalize after three to nine months46-48. Neither testis strictly diagnostic of infection, but abnormalities in the absenceof other inflammatory states should raise the surgeon’s index ofsuspicion.

Joint AspirationThere are no rigorous, large-scale investigations available thataddress the following questions: (1) When is it appropriate todiagnostically aspirate a shoulder with a prosthetic joint? (2) Ifthe decision is made to aspirate the shoulder prior to, or during,revision arthroplasty, what values of the synovial fluid leukocytecount are predictive of an infection?

Evidence-based Clinical Practice Guidelines published bythe American Academy of Orthopaedic Surgeons (AAOS) re-commend proceeding with joint aspiration in a patient with apain in the hip or knee after arthroplasty and an elevated ESRand CRP4. This is based on the observation that the ESR andCRP have a high positive predictive value and sensitivity for thepresence of infection after hip and knee arthroplasty. If theseserologic tests are elevated in a patient dissatisfied with his orher shoulder replacement, it remains prudent to follow theAAOS guidelines. If the serologic tests are normal, the decisionto aspirate a shoulder with a prosthetic joint remains largely basedon the judgment of the evaluating surgeon.

Synovial Leukocyte CountsStrict thresholds for diagnostic synovial leukocyte counts arestill an active area of debate6. Bauer et al. suggested that a peri-prosthetic synovial fluid white blood-cell count of >500 cells/mLis suggestive of an infection29. However, an accurate threshold valuemay be unique to each joint. To complicate the situation, in patientswith P. acnes infections, there is rarely enough periprosthetic fluidpresent to complete a leukocyte cell count27, and when there is,the test is frequently normal41.

Fig. 2-A Fig. 2-B

Figs.2-A and 2-B Axillary lateral radiographsof a patientwho had a reverse total shoulderarthroplasty and wasseen with periprosthetic loosening confirmed

via intraoperative cultures to be caused by a late P. acnes infection. Fig. 2-A Radiograph made immediately postoperatively. Fig. 2-B Radiograph,

made eight years postoperatively, demonstrates changes, including generalized bone resorption of the proximal part of the humerus (asterisks) and

periprosthetic radiolucencies adjacent to both the humerosocket and glenosphere components (arrows), that occurred over time.

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Synovial Fluid CultureAlthough synovial leukocyte counts appear to be of minimalvalue most of the time, any fluid samples obtained should besent for aerobic and anaerobic bacterial cultures. Kowalski et el.pooled the results of five studies on infection after shoulderarthroplasty and showed that as many as two-thirds of patients(thirty-three of fifty) may have positive preoperative joint as-piration cultures49. However, the majority of the patients inthose series presented with overt signs of infection. Patientswith overt signs of infection are likely to yield cultures that arepositive for microorganisms other than P. acnes or coagulase-negative Staphylococcus.

Intraoperative FindingsHistological AnalysisIntraoperative findings are not often helpful, especially whenless virulent organisms such as P. acnes or coagulase-negativeStaphylococcus are eventually identified. Frozen sections of biopsyspecimens of periprosthetic membrane or the joint capsuleare the most commonly used intraoperative tests to evaluatefor infection. Historically, the criterion indicative of acute in-flammation most likely to be associated with an underlyingperiprosthetic infection was described by Mirra et al. as greaterthan five neutrophils in five or more high-power microscopicfields50. This criterion has been validated by high-level clini-cal evidence in the setting of lower-extremity periprostheticjoint infection39,51-57. It should also be noted that the results ofthese histologic samples may be skewed with inflammatoryarthropathy.

With regard to the shoulder, most studies have notshown a positive correlation between intraoperative frozen-section findings and eventual positive culture results in caseswhen frank purulence is not encountered. Topolski et al. ret-rospectively evaluated the value of intraoperative histologicalanalysis in seventy-five shoulders that underwent revisionarthroplasty and eventually yielded positive culture results,finding that only 8% (six) of seventy-three patients with dataavailable had acute inflammation at the time of the revision44.The majority of their cultures resulted in growth of P. acnes(60%; forty-five of seventy-five patients), followed by Staphy-lococcus epidermidis (13%; ten patients), and three other spe-cies. The importance of the majority of these positive culturesremains unknown as treatments varied considerably and onlyten patients required an additional revision surgery. In a large-scale review of factors prognostic for a positive cultures fol-lowing revision shoulder arthroplasty, Pottinger et al. did notfind either acute or chronic inflammation to be predictive ofthe growth of P. acnes or other organisms24. In a series oftwenty-eight revision arthroplasties in shoulders presumed tobe uninfected, Kelly and Hobgood reported that 29% (eight)had positive cultures41. Six of those patients were positive forP. acnes and only 4% (one patient) had acute inflammationintraoperatively. Their experience indicates that there are cur-rently no preoperative or intraoperative findings that are reli-ably predictive of eventual culture growth by less virulentorganisms.

Microbiologic TestingRepresentative periprosthetic tissue and synovial fluid culturesare considered the gold standard for determining the presenceof a periprosthetic shoulder infection. However, while they arethe reference standard, periprosthetic cultures are sensitiveto the prevalence of a given condition and its pretest proba-bility. The importance of pretest probability and prevalence asthey relate to periprosthetic cultures has been demonstratedin hip58 and knee59 arthroplasty, and presents a critical problemin the setting of the shoulder—it is difficult to narrow downwhich patients have a higher likelihood of infection because ofthe poor sensitivity and specificity of the available screeningtests. A detailed discussion of the importance of prevalence as itrelates to the value of a diagnostic test as well as future direc-tions for diagnostic testing is available in the Appendix.

Unfortunately, the traditionally utilized screening testsare surrogates for the inflammatory response caused by the ab-normal presence of pathogenic microbes. While it may be animportant cause of morbidity, P. acnes does not seem to elicit thislevel of inflammatory response and these inflammatory markershave not been proven to be useful. However, Pottinger et al.demonstrated that male sex, cloudy synovial fluid, humeralosteolysis and loosening, glenoid wear, and periprosthetic mem-brane formation are associated with an increased likelihood ofpositive P. acnes culture growth24.

The optimal duration of culture incubation has also notbeen agreed on. P. acnes may require as long as three weeksto be isolated in culture, with average culture times reportedto range from seven to thirteen days27,42. Many authors haveagreed that specimens should be held for at least fourteen daysto allow for the growth of P. acnes27,42,60-62. However, it has alsobeen recommended that cultures be observed for at leasttwenty-eight days24. The balance between maximizing culturesensitivity and minimizing the risk of contamination with regardto the duration of incubation must be evaluated before evidence-based recommendations can be made. No specific culture me-dium has been demonstrated to be superior in the detection offastidious microorganisms like P. acnes, although optimumsensitivity requires both aerobic and anaerobic conditions60.

ClassificationCategorization of the type of periprosthetic shoulder infectionis important in determining the most appropriate treatmentand prognosis. This can be done on the basis of the most likelyroute of infection and the timing (Table III). The traditionalclassification of periprosthetic shoulder infection25,63,64 fails toinclude a category for the common and more frequently en-countered situation: late culture positivity with an organismof low virulence (e.g., P. acnes, coagulase-negative Staphylo-coccus, and Corynebacterium species). This clinical scenariodoes not fit neatly into the traditional classification schemebecause neither the timing nor the route of infection is confi-dently known. In fact, given the concern for false positives andthe lack of other diagnostic tests to confirm the culture data,whether these positive cultures are pathologic in nature is notalways clear.

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To include this clinical scenario and improve future out-comes analyses, we propose an additional acronym to thisclassification scheme: FAPC—failed arthroplasty with positivecultures. The proportion of positive cultures of those collectedshould also be reported as a distinct outcome. For example,a patient with one of five cultures positive for P. acnes or fourof five cultures positive for P. acnes should be reported as FAPC1/5 for P. acnes or FAPC 4/5 for P. acnes, respectively. Thisreporting scheme will remind surgeons that shoulder painafter arthroplasty must be evaluated for the presence of low-virulence microbes. It will also allow for the pooling of theresults of future investigations to help elucidate the importanceof these positive culture results to the clinical outcomes ofrevision surgery.

ManagementOnce it is decided that infection is the most likely etiology forshoulder arthroplasty failure, surgery is the mainstay of treat-ment. The first step is to thoroughly evaluate the patient’smedical history and current medical status to assess his or herability to successfully undergo one or more surgical proce-dures. Treatment options include antibiotic suppression, irri-gation and debridement with prosthesis retention, resectionarthroplasty, one-stage exchange, staged reimplantation, ar-throdesis, and amputation (see Appendix).

Coste et al. reported their experience with the use ofantibiotic treatment alone to treat five periprosthetic shoulderinfections65. They found that symptomatic infection was persis-tent in three of five shoulders. The results of similar treatmentin the hip and knee are even more dismal, with failure ratesexceeding 75%66. These results are not encouraging; therefore,antibiotic suppression alone is likely only an option for a patientunfit to undergo general anesthesia and whose surgical risks areexcessive because of medical comorbidities.

Antibiotic treatment is an essential adjuvant to surgicaltreatment alternatives and should be tailored to fit the sus-ceptibility of microorganisms identified in culture. High-levelevidence regarding antibiotic type, route, dose, and durationare lacking; therefore, these decisions should be made in con-cert with a medical infectious disease consultant. General rec-ommendations regarding pathogen-specific antimicrobial agentsof choice are given in the Appendix.

When weighing the risks and benefits of the surgicaloptions available, the patient and surgeon must consider thepatient’s preoperative functional status, expectations, and riskof recurrence on the basis of the type and duration of theinfection. Clearance of infection is the sine qua non for anyattempt at reconstruction to succeed. It is critical to beware ofmore virulent organisms, such as Staphylococcus aureus, or alonger duration of symptoms, because, in the hip and kneearthroplasty experience, these are independent predictors oftreatment failure67. Both Coste et al.65 and Sperling et al.25 re-ported their experience with debridement and implant reten-tion (see Appendix), with recurrence rates of 12% and 50%,respectively. Their results further highlight the enigma of theFAPC: the importance of the positive cultures at the time ofrevision is often unknown; therefore, consensus is lacking inhow to reliably and reproducibly evaluate the treatment out-comes. Although Coste et al. reported a low recurrence rate,63% of their patients required revision surgery and functionaloutcomes remained poor. This approach is rarely indicated,given that the majority of periprosthetic shoulder infectionspresent in a subacute or chronic manner25,65,68-73.

In the patient with low functional demands and expec-tations, a higher surgical risk, extensive bone loss followingdebridement, and/or the desire to avoid more than one pro-cedure, resection arthroplasty may be the most suitable option.Resection arthroplasty can provide pain relief in addition to

TABLE III Modified Classification of Periprosthetic Shoulder Infections*

Classification Characteristics

Route of infectionPerioperative Inoculation of pathogens during or immediately after index procedureHematogenous Through blood or lymph spread from a distant site of infection (e.g., urinary tract infection,

pneumonia, and oral abscess)Contiguous Spread from an adjacent source of infection (e.g., skin or soft-tissue abscess, osteomyelitic

sequestrum, and preexisting septic arthritis)

TimingAcute (<3 mos) Often caused by highly virulent microbes (e.g., Staphylococcus aureus, Streptococcus species,

and gram-negative bacilli) that stimulate a pyogenic immune responseSubacute (3-12 mos) Potentially acquired during prosthesis implantation; predominantly less virulent pathogens

(e.g., P. acnes and coagulase-negative Staphylococcus species)Late (>12 mos) Potentially caused by hematogenous seeding or a less virulent pathogen (see above)

FAPC (X/Y for Z)† Timing and route of potential infection unknown; delayed culture growth by an organism with lowvirulence (e.g., P. acnes, coagulase-negative Staphylococcus species, and Corynebacterium species)

*The classifications are based on previous descriptions by Sperling et al.25, Wolfe et al.63, and Yamaguchi et al.64. †FAPC = failed arthroplasty withpositive cultures, X = number of positive cultures, Y = total number of cultures specimens taken, and Z = microorganism identified in culture.

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low rates of infection recurrence, frequently at the expense offunction74. Infection recurrence rates have been reported torange from 0% to 30%65,68,72,73,75,76. Crosby et al. demonstratedthat surgeon-constructed and commercially available articu-lating cement spacers impregnated with vancomycin alone orin combination with an aminoglycoside are both effective treat-ment techniques77-79. Articulating antibiotic cement spacers allowfor the preservation of a soft-tissue envelope and can often actas the definitive implant in a patient with minimal functionaldemands80. On the basis of these findings, we adopted thisstaged revision strategy at our institution and recommend theaddition of vancomycin to gentamicin-impregnated cement forbroader gram-positive pathogen coverage. In a younger patientwith higher demands, arthrodesis may be a more suitable op-tion. Nevertheless, substantial bone loss in these patients canlead to a challenging situation that frequently requires multiplesurgical revision procedures and vascularized fibular autograftto achieve fusion81.

One-stage exchange arthroplasty has also been investi-gated, with promising results. The advantages of one-stagesurgery include less destruction and/or dissection, immediatereconstruction, avoidance of secondary adhesions, less patientangst, and lower hospitalization cost82. Ince et al.69 reportedtheir results in treating predominantly subacute and late in-fections utilizing this method. They were able to successfullymanage FAPCs in their small series and reported that thesubjective outcomes were at least as successful as the reportedresults of resection arthroplasty or two-stage exchange. Suc-cessful management was defined as improvement with regardto pain and the absence of implant failure, although no at-tempt was made to determine if bacteria remained around theprosthetic joint.

Modeled after what has been demonstrated in the hipand knee arthroplasty literature83,84, two-stage reimplantation,in which all original prosthetic components and associatedcement are removed in the initial stage, has become the treat-ment of choice because of the low rate of persistent infectionand most optimal functional outcomes. Success rates for in-fection clearance have been reported to range from 0% to36%25,65,71,73,77,85,86, and systematic review of the literature onperiprosthetic infections of the hip and knee has also con-firmed the superiority of two-stage protocols87. Nonetheless,both the surgeon and the patient should be aware that thesubjective outcomes of revision for infection are the least fa-vorable compared with revisions for any other indication85.

It is recommended that all cement, necrotic or infectedsoft tissue, synovial lining, and bone be debrided; therefore,osseous as well as soft-tissue deficits following glenohumeralinfections can pose a substantial reconstructive challenge. Thiscan require muscle transfers or even pedicled myocutaneousflaps for coverage88. Preservation of functional rotator cufftissue to allow for an adequate force couple is a frequentproblem for which reverse total shoulder arthroplasty may behelpful. Several authors have investigated the use of reversetotal shoulder arthroplasty in this setting70,89 and have shown arelatively low risk of recurrent infection, improved function,

and reduced pain. Recurrence rates have been reported to rangefrom 0% to 6% whether this is done in a single89 or staged70,89

fashion. Similar to the use of the reverse total shoulder ar-throplasty design for other indications, complication rates arehigh90. Periprosthetic shoulder infection has been reported tobe more common following reverse total shoulder arthroplastythan after the use of unconstrained designs91,92, whether per-formed in the primary93 or revision94 scenario. Therefore, pa-tients should be cautioned with regard to the high likelihoodfor revision surgery if this approach is utilized89.

OverviewPeriprosthetic infection is a devastating complication followingshoulder arthroplasty that presents numerous diagnostic,treatment, and technical challenges for both the patient and theclinician. The unique profile of the microbial pathogens ofthe shoulder is responsible for many of these challenges. Witha clinical picture that is equivocal, no signs of suppurative in-fection at surgery, no reliable screening test, and no reliableintraoperative test, surgeons are left with only the delayedresults of operative cultures to determine the presence ofless virulent organisms and to make the diagnosis of FAPC.However, the true importance of these positive cultures inFAPC remains unclear. Key test characteristics, such as thefalse-positive rate and the prevalence of positive culturesin well-performing shoulders, are unknown as there is nouseful confirmatory test to validate the culture data and noreliable way to detect the presence of less virulent microor-ganisms without reoperation. The ability to obtain a promptand accurate diagnosis is paramount to improving out-comes. The lessons learned from the study of periprostheticinfections after hip and knee arthroplasty continue to serveas an example of how evidence-based recommendations arecritical in the prevention, identification, and treatment ofthis vexing problem, but further research is needed to tacklethe unique challenges presented by periprosthetic shoulderinfection.

AppendixTables showing the outcomes of the treatment of peri-prosthetic shoulder infections reported in the literature,

the most common microbes responsible for periprostheticinfections of the hip and knee, the MusculoSkeletal InfectionSociety definition of periprosthetic joint infection, the effect ofinfection prevalence on the predictive value of a diagnostic test,and the antibiotic treatment recommendations for commonmicroorganisms identified in periprosthetic shoulder infec-tions; in addition, detailed discussions regarding the uniquemicrobiologic profile of the shoulder and the challenges toarriving at a universally accepted definition of a periprostheticshoulder infection, the importance of the prevalence of peri-prosthetic infection as it relates to the value of a diagnostic test,and the future directions for diagnostic testing (including ref-erences 95 through 124, which are cited only in the Appendix)are available with the online version of this article as a datasupplement at jbjs.org. n

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William R. Mook, MDGrant E. Garrigues, MDDepartment of Orthopaedic Surgery,

Duke University Medical Center, Box 3000,Durham, NC 27710.E-mail address for W.R. Mook: [email protected]

References

1. Kim SH, Wise BL, Zhang Y, Szabo RM. Increasing incidence of shoulder arthro-plasty in the United States. J Bone Joint Surg Am. 2011 Dec 21;93(24):2249-54.2. Day JS, Lau E, Ong KL, Williams GR, Ramsey ML, Kurtz SM. Prevalence andprojections of total shoulder and elbow arthroplasty in the United States to 2015.J Shoulder Elbow Surg. 2010 Dec;19(8):1115-20. Epub 2010 Jun 15.3. Della Valle C, Parvizi J, Bauer TW, Dicesare PE, Evans RP, Segreti J, Spangehl M,Watters WC 3rd, Keith M, Turkelson CM, Wies JL, Sluka P, Hitchcock K; AmericanAcademy of Orthopaedic Surgeons. Diagnosis of periprosthetic joint infections of thehip and knee. J Am Acad Orthop Surg. 2010 Dec;18(12):760-70.4. Della Valle C, Parvizi J, Bauer TW, DiCesare PE, Evans RP, Segreti J, Spangehl M,Watters WC 3rd, Keith M, Turkelson CM, Wies JL, Sluka P, Hitchcock K; AmericanAcademy of Orthopaedic Surgeons. American Academy of Orthopaedic Surgeonsclinical practice guideline on: the diagnosis of periprosthetic joint infections of thehip and knee. J Bone Joint Surg Am. 2011 Jul 20;93(14):1355-7.5. Parvizi J. New definition for periprosthetic joint infection. Am J Orthop (Belle MeadNJ). 2011 Dec;40(12):614-5.6. Parvizi J, Zmistowski B, Berbari EF, Bauer TW, Springer BD, Della Valle CJ,Garvin KL, Mont MA, Wongworawat MD, Zalavras CG. New definition for peri-prosthetic joint infection: from the Workgroup of the Musculoskeletal InfectionSociety. Clin Orthop Relat Res. 2011 Nov;469(11):2992-4.7. Bohsali KI, Wirth MA, Rockwood CA Jr. Complications of total shoulder arthro-plasty. J Bone Joint Surg Am. 2006 Oct;88(10):2279-92.8. Cofield RH, Edgerton BC. Total shoulder arthroplasty: complications and revisionsurgery. Instr Course Lect. 1990;39:449-62.9. Crowninshield RD, Rosenberg AG, Sporer SM. Changing demographics ofpatients with total joint replacement. Clin Orthop Relat Res. 2006 Feb;443(443):266-72.10. Ong KL, Mowat FS, Chan N, Lau E, Halpern MT, Kurtz SM. Economic burden ofrevision hip and knee arthroplasty in Medicare enrollees. Clin Orthop Relat Res.2006 May;446(446):22-8.11. Wright JG, Einhorn TA, Heckman JD. Grades of recommendation. J Bone JointSurg Am. 2005 Sep;87(9):1909-10.12. Dowsey MM, Choong PF. Obese diabetic patients are at substantial risk fordeep infection after primary TKA. Clin Orthop Relat Res. 2009 Jun;467(6):1577-81.Epub 2008 Oct 8.13. Jamsen E, Varonen M, Huhtala H, Lehto MU, Lumio J, Konttinen YT, Moilanen T.Incidence of prosthetic joint infections after primary knee arthroplasty. J Arthro-plasty. 2010 Jan;25(1):87-92. Epub 2008 Dec 4.14. Ong KL, Kurtz SM, Lau E, Bozic KJ, Berry DJ, Parvizi J. Prosthetic joint infectionrisk after total hip arthroplasty in the Medicare population. J Arthroplasty. 2009Sep;24(6)(Suppl):105-9. Epub 2009 Jun 2.15. Samson AJ, Mercer GE, Campbell DG. Total knee replacement in the morbidlyobese: a literature review. ANZ J Surg. 2010 Sep;80(9):595-9. Epub 2010 Aug 19.16. Marchant MH Jr, Viens NA, Cook C, Vail TP, Bolognesi MP. The impact of gly-cemic control and diabetes mellitus on perioperative outcomes after total joint ar-throplasty. J Bone Joint Surg Am. 2009 Jul;91(7):1621-9.17. Drancourt M, Argenson JN, Tissot Dupont H, Aubaniac JM, Raoult D. Psoriasis isa risk factor for hip-prosthesis infection. Eur J Epidemiol. 1997 Feb;13(2):205-7.18. Lehman CR, Ries MD, Paiement GD, Davidson AB. Infection after total jointarthroplasty in patients with human immunodeficiency virus or intravenous drug use.J Arthroplasty. 2001 Apr;16(3):330-5.19. Jeys LM, Grimer RJ, Carter SR, Tillman RM. Periprosthetic infection in patientstreated for an orthopaedic oncological condition. J Bone Joint Surg Am. 2005Apr;87(4):842-9.20. Berbari EF, Hanssen AD, Duffy MC, Steckelberg JM, Ilstrup DM, Harmsen WS,Osmon DR. Risk factors for prosthetic joint infection: case-control study. Clin InfectDis. 1998 Nov;27(5):1247-54.21. Cheung EV, Sperling JW, Cofield RH. Infection associated with hematoma for-mation after shoulder arthroplasty. Clin Orthop Relat Res. 2008 Jun;466(6):1363-7.Epub 2008 Apr 18.22. Singh JA, Sperling JW, Schleck C, Harmsen W, Cofield RH. Periprostheticinfections after shoulder hemiarthroplasty. J Shoulder Elbow Surg. 2012Oct;21(10):1304-9. Epub 2011 Dec 11.23. Singh JA, Sperling JW, Schleck C, Harmsen WS, Cofield RH. Periprostheticinfections after total shoulder arthroplasty: a 33-year perspective. J Shoulder ElbowSurg. 2012 Nov;21(11):1534-41. Epub 2012 Apr 18.24. Pottinger P, Butler-Wu S, Neradilek MB, Merritt A, Bertelsen A, Jette JL, Warme WJ,Matsen FA 3rd. Prognostic factors for bacterial cultures positive for Propionibacteriumacnes and other organisms in a large series of revision shoulder arthroplasties

performed for stiffness, pain, or loosening. J Bone Joint Surg Am. 2012 Nov 21;94(22):2075-83.25. Sperling JW, Kozak TK, Hanssen AD, Cofield RH. Infection after shoulderarthroplasty. Clin Orthop Relat Res. 2001 Jan;(382):206-16.26. Dodson CC, Craig EV, Cordasco FA, Dines DM, Dines JS, Dicarlo E, Brause BD,Warren RF. Propionibacterium acnes infection after shoulder arthroplasty: a diag-nostic challenge. J Shoulder Elbow Surg. 2010 Mar;19(2):303-7. Epub 2009 Nov 1.27. Millett PJ, Yen YM, Price CS, Horan MP, van der Meijden OA, Elser F. Propioni-bacterium acnes infection as an occult cause of postoperative shoulder pain: a caseseries. Clin Orthop Relat Res. 2011 Oct;469(10):2824-30. Epub 2011 Jan 15.28. Tigges S, Stiles RG, Roberson JR. Appearance of septic hip prostheses on plainradiographs. AJR Am J Roentgenol. 1994 Aug;163(2):377-80.29. Bauer TW, Parvizi J, Kobayashi N, Krebs V. Diagnosis of periprosthetic infection.J Bone Joint Surg Am. 2006 Apr;88(4):869-82.30. Zimmerli W, Trampuz A, Ochsner PE. Prosthetic-joint infections. N Engl J Med.2004 Oct 14;351(16):1645-54.31. Levitsky KA, Hozack WJ, Balderston RA, Rothman RH, Gluckman SJ, Maslack MM,Booth RE Jr. Evaluation of the painful prosthetic joint. Relative value of bone scan,sedimentation rate, and joint aspiration. J Arthroplasty. 1991 Sep;6(3):237-44.32. Scher DM, Pak K, Lonner JH, Finkel JE, Zuckerman JD, Di Cesare PE. Thepredictive value of indium-111 leukocyte scans in the diagnosis of infected total hip,knee, or resection arthroplasties. J Arthroplasty. 2000 Apr;15(3):295-300.33. Stumpe KD, Notzli HP, Zanetti M, Kamel EM, Hany TF, Gorres GW, vonSchulthess GK, Hodler J. FDG PET for differentiation of infection and aseptic loos-ening in total hip replacements: comparison with conventional radiography andthree-phase bone scintigraphy. Radiology. 2004 May;231(2):333-41. Epub 2004Mar 24.34. Teller RE, Christie MJ, Martin W, Nance EP, Haas DW. Sequential indium-labeledleukocyte and bone scans to diagnose prosthetic joint infection. Clin Orthop RelatRes. 2000 Apr;(373):241-7.35. Zhuang H, Duarte PS, Pourdehnad M, Maes A, Van Acker F, Shnier D, Garino JP,Fitzgerald RH, Alavi A. The promising role of 18F-FDG PET in detecting infected lowerlimb prosthesis implants. J Nucl Med. 2001 Jan;42(1):44-8.36. Huo MH, Stockton KG, Mont MA, Parvizi J. What’s new in total hip arthroplasty.J Bone Joint Surg Am. 2010 Dec 15;92(18):2959-72.37. Parvizi J, Ghanem E, Sharkey P, Aggarwal A, Burnett RS, Barrack RL. Diagnosisof infected total knee: findings of a multicenter database. Clin Orthop Relat Res.2008 Nov;466(11):2628-33. Epub 2008 Sep 10.38. Greidanus NV, Masri BA, Garbuz DS, Wilson SD, McAlinden MG, Xu M, DuncanCP. Use of erythrocyte sedimentation rate and C-reactive protein level to diagnoseinfection before revision total knee arthroplasty. A prospective evaluation. J BoneJoint Surg Am. 2007 Jul;89(7):1409-16.39. Schinsky MF, Della Valle CJ, Sporer SM, Paprosky WG. Perioperative testing forjoint infection in patients undergoing revision total hip arthroplasty. J Bone Joint SurgAm. 2008 Sep;90(9):1869-75.40. Cheung EV, Sperling JW, Cofield RH. Revision shoulder arthroplasty for glenoidcomponent loosening. J Shoulder Elbow Surg. 2008 May-Jun;17(3):371-5. Epub2008 Feb 20.41. Kelly JD 2nd, Hobgood ER. Positive culture rate in revision shoulder arthro-plasty. Clin Orthop Relat Res. 2009 Sep;467(9):2343-8. Epub 2009 May 12.42. Lutz MF, Berthelot P, Fresard A, Cazorla C, Carricajo A, Vautrin AC, Fessy MH,Lucht F. Arthroplastic and osteosynthetic infections due to Propionibacterium acnes:a retrospective study of 52 cases, 1995-2002. Eur J Clin Microbiol Infect Dis. 2005Nov;24(11):739-44.43. Piper KE, Jacobson MJ, Cofield RH, Sperling JW, Sanchez-Sotelo J, Osmon DR,McDowell A, Patrick S, Steckelberg JM, Mandrekar JN, Fernandez Sampedro M,Patel R. Microbiologic diagnosis of prosthetic shoulder infection by use of implantsonication. J Clin Microbiol. 2009 Jun;47(6):1878-84. Epub 2009 Mar 4.44. Topolski MS, Chin PY, Sperling JW, Cofield RH. Revision shoulder arthroplastywith positive intraoperative cultures: the value of preoperative studies and intra-operative histology. J Shoulder Elbow Surg. 2006 Jul-Aug;15(4):402-6.45. Zeller V, Ghorbani A, Strady C, Leonard P, Mamoudy P, Desplaces N. Propioni-bacterium acnes: an agent of prosthetic joint infection and colonization. J Infect.2007 Aug;55(2):119-24. Epub 2007 Apr 5.46. Bilgen O, Atici T, Durak K, Karaeminogullari, Bilgen MS. C-reactive proteinvalues and erythrocyte sedimentation rates after total hip and total knee arthro-plasty. J Int Med Res. 2001 Jan-Feb;29(1):7-12.47. Larsson S, Thelander U, Friberg S. C-reactive protein (CRP) levels after electiveorthopedic surgery. Clin Orthop Relat Res. 1992 Feb;(275):237-42.

963

TH E J O U R N A L O F B O N E & JO I N T SU R G E RY d J B J S . O R G

VO LU M E 96-A d NU M B E R 11 d J U N E 4, 2014DI AG N O S I S A N D MA N AG E M E N T O F P E R I P R O S T H E T I C

SH O U L D E R IN F E C T I O N S

Page 9: Periprosthetic Shoulder Infections

48. Park KK, Kim TK, Chang CB, Yoon SW, Park KU. Normative Temporal Values ofCRP and ESR in Unilateral and Staged Bilateral TKA. Clin Orthop Relat Res. 2008Jan;466(1):179-88. Epub 2008 Jan 3.49. Kowalski TJ, Berbari EF, Osmon DR. Medical evaluation and treatment for infectionin shoulder arthroplasty. In: Cofield RH, Sperling JW, editors. Revision and complexshoulder arthoplasty. Philadelphia: Lippincott Williams & Wilkins; 2010. p 47-54.50. Mirra JM, Amstutz HC, Matos M, Gold R. The pathology of the joint tissues andits clinical relevance in prosthesis failure. Clin Orthop Relat Res. 1976Jun;(117):221-40.51. Banit DM, Kaufer H, Hartford JM. Intraoperative frozen section analysis inrevision total joint arthroplasty. Clin Orthop Relat Res. 2002 Aug;(401):230-8.52. Della Valle CJ, Sporer SM, Jacobs JJ, Berger RA, Rosenberg AG, Paprosky WG.Preoperative testing for sepsis before revision total knee arthroplasty. J Arthroplasty.2007 Sep;22(6)(Suppl 2):90-3. Epub 2007 Jul 26.53. Fehring TK, McAlister JA Jr. Frozen histologic section as a guide to sepsisin revision joint arthroplasty. Clin Orthop Relat Res. 1994 Jul;(304):229-37.54. Frances Borrego A, Martınez FM, Cebrian Parra JL, Graneda DS, Crespo RG, Lopez-Duran Stern L. Diagnosis of infection in hip and knee revision surgery: intraoperativefrozen section analysis. Int Orthop. 2007 Feb;31(1):33-7. Epub 2006 Mar 18.55. Ko PS, Ip D, Chow KP, Cheung F, Lee OB, Lam JJ. The role of intraoperativefrozen section in decision making in revision hip and knee arthroplasties in a localcommunity hospital. J Arthroplasty. 2005 Feb;20(2):189-95.56. Lonner JH, Desai P, Dicesare PE, Steiner G, Zuckerman JD. The reliability ofanalysis of intraoperative frozen sections for identifying active infection during re-vision hip or knee arthroplasty. J Bone Joint Surg Am. 1996 Oct;78(10):1553-8.57. Nunez LV, Buttaro MA, Morandi A, Pusso R, Piccaluga F. Frozen sections ofsamples taken intraoperatively for diagnosis of infection in revision hip surgery. ActaOrthop. 2007 Apr;78(2):226-30.58. Barrack RL, Harris WH. The value of aspiration of the hip joint before revisiontotal hip arthroplasty. J Bone Joint Surg Am. 1993 Jan;75(1):66-76.59. Barrack RL. The value of preoperative knee aspiration: don’t ask, don’t tell.Orthopedics. 1997 Sep;20(9):862-4.60. Butler-Wu SM, Burns EM, Pottinger PS, Magaret AS, Rakeman JL, Matsen FA3rd, Cookson BT. Optimization of periprosthetic culture for diagnosis of Propioni-bacterium acnes prosthetic joint infection. J Clin Microbiol. 2011.61. Schafer P, Fink B, Sandow D, Margull A, Berger I, Frommelt L. Prolonged bac-terial culture to identify late periprosthetic joint infection: a promising strategy. ClinInfect Dis. 2008 Dec 1;47(11):1403-9.62. Morman M, Fowler RL, Sanofsky B, Higgins LD. Arthroscopic tissue biopsy forevaluation of infection before revision arthroplasty. J Shoulder Elbow Surg. 2011Apr;20(3):e15-22. Epub 2011 Feb 18.63. Wolfe SW, Figgie MP, Inglis AE, Bohn WW, Ranawat CS. Management of infec-tion about total elbow prostheses. J Bone Joint Surg Am. 1990 Feb;72(2):198-212.64. Yamaguchi K, Adams RA, Morrey BF. Infection after total elbow arthroplasty.J Bone Joint Surg Am. 1998 Apr;80(4):481-91.65. Coste JS, Reig S, Trojani C, Berg M, Walch G, Boileau P. The management ofinfection in arthroplasty of the shoulder. J Bone Joint Surg Br. 2004 Jan;86(1):65-9.66. Hanssen AD, Rand JA. Evaluation and treatment of infection at the site of a totalhip or knee arthroplasty. Instr Course Lect. 1999;48:111-22.67. Marculescu CE, Berbari EF, Hanssen AD, Steckelberg JM, Harmsen SW,Mandrekar JN, Osmon DR. Outcome of prosthetic joint infections treated with de-bridement and retention of components. Clin Infect Dis. 2006 Feb 15;42(4):471-8.Epub 2006 Jan 5.68. Braman JP, Sprague M, Bishop J, Lo IK, Lee EW, Flatow EL. The outcome ofresection shoulder arthroplasty for recalcitrant shoulder infections. J Shoulder ElbowSurg. 2006 Sep-Oct;15(5):549-53. Epub 2006 Aug 7.69. Ince A, Seemann K, Frommelt L, Katzer A, Loehr JF. One-stage exchange shoulderarthroplasty for peri-prosthetic infection. J Bone Joint Surg Br. 2005 Jun;87(6):814-8.70. Sabesan VJ, Ho JC, Kovacevic D, Iannotti JP. Two-stage reimplantation fortreating prosthetic shoulder infections. Clin Orthop Relat Res. 2011 Sep;469(9):2538-43.71. Strickland JP, Sperling JW, Cofield RH. The results of two-stage re-implantationfor infected shoulder replacement. J Bone Joint Surg Br. 2008 Apr;90(4):460-5.72. Verhelst L, Stuyck J, Bellemans J, Debeer P. Resection arthroplasty of theshoulder as a salvage procedure for deep shoulder infection: does the use ofa cement spacer improve outcome? J Shoulder Elbow Surg. 2011 Dec;20(8):1224-33. Epub 2011 May 20.73. Weber P, Utzschneider S, Sadoghi P, Andress HJ, Jansson V, Muller PE. Man-agement of the infected shoulder prosthesis: a retrospective analysis and review ofthe literature. Int Orthop. 2011 Mar;35(3):365-73. Epub 2010 Apr 20.74. Mileti J, Sperling JW, Cofield RH. Reimplantation of a shoulder arthroplasty after aprevious infected arthroplasty. J Shoulder Elbow Surg. 2004 Sep-Oct;13(5):528-31.75. Muh SJ, Streit JJ, Lenarz CJ, McCrum C, Wanner JP, Shishani Y, Moraga C,Nowinski RJ, Edwards TB, Warner JJ, Walch G, Gobezie R. Resection arthroplasty forfailed shoulder arthroplasty. J Shoulder Elbow Surg. 2013 Feb;22(2):247-52. Epub2012 Aug 29.

76. Rispoli DM, Sperling JW, Athwal GS, Schleck CD, Cofield RH. Pain relief andfunctional results after resection arthroplasty of the shoulder. J Bone Joint Surg Br.2007 Sep;89(9):1184-7.77. Coffey MJ, Ely EE, Crosby LA. Treatment of glenohumeral sepsis with a com-mercially produced antibiotic-impregnated cement spacer. J Shoulder Elbow Surg.2010 Sep;19(6):868-73. Epub 2010 Apr 14.78. Crosby LA. Infected total shoulder arthroplasty: two-stage revision. In: Zuckerman JD,editor. Advanced reconstruction: shoulder. Rosemont: American Academy of OrthopaedicSurgeons; 2007. p 605-611.79. Gorman MT, Crosby LA. Treatment of deep infection after total shoulder ar-throplasty with an antibiotic-impregnated cement spacer. Tech Shoulder Elbow Surg.2006:7:782-5.80. Themistocleous G, Zalavras C, Stine I, Zachos V, Itamura J. Prolonged im-plantation of an antibiotic cement spacer for management of shoulder sepsis incompromised patients. J Shoulder Elbow Surg. 2007 Nov-Dec;16(6):701-5. Epub2007 Oct 10.81. Bilgin SS. Reconstruction of proximal humeral defects with shoulder arthrod-esis using free vascularized fibular graft. J Bone Joint Surg Am. 2012 Jul 3;94(13):e94.82. Joachim L. Surgical Management of the Infected Shoulder Arthoplasty. In:Cofield RH, Sperling JW, editors. Revision and complex shoulder arthroplasty.Philadelphia: Lippincott Williams & Wilkins; 2010. p 214-223.83. Garvin KL, Hanssen AD. Infection after total hip arthroplasty. Past, present, andfuture. J Bone Joint Surg Am. 1995 Oct;77(10):1576-88.84. Jamsen E, Stogiannidis I, Malmivaara A, Pajamaki J, Puolakka T, Konttinen YT.Outcome of prosthesis exchange for infected knee arthroplasty: the effect of treat-ment approach. Acta Orthop. 2009 Feb;80(1):67-77.85. Dines JS, Fealy S, Strauss EJ, Allen A, Craig EV, Warren RF, Dines DM. Out-comes analysis of revision total shoulder replacement. J Bone Joint Surg Am. 2006Jul;88(7):1494-500.86. Seitz WH Jr, Damacen H. Staged exchange arthroplasty for shoulder sepsis.J Arthroplasty. 2002 Jun;17(4)(Suppl 1):36-40.87. Lange J, Troelsen A, Thomsen RW, Søballe K. Chronic infections in hip arthro-plasties: comparing risk of reinfection following one-stage and two-stage revision:a systematic review and meta-analysis. Clin Epidemiol. 2012;4:57-73. Epub 2012Mar 27.88. Heitmann C, Higgins LD, Levin LS. Treatment of deep infections of the shoulderwith pedicled myocutaneous flaps. J Shoulder Elbow Surg. 2004 Jan-Feb;13(1):13-7.89. Cuff DJ, Virani NA, Levy J, Frankle MA, Derasari A, Hines B, Pupello DR, Cancio M,Mighell M. The treatment of deep shoulder infection and glenohumeral instabilitywith debridement, reverse shoulder arthroplasty and postoperative antibiotics.J Bone Joint Surg Br. 2008 Mar;90(3):336-42.90. Cheung E, Willis M, Walker M, Clark R, Frankle MA. Complications in reversetotal shoulder arthroplasty. J Am Acad Orthop Surg. 2011 Jul;19(7):439-49.91. Fehringer EV, Mikuls TR, Michaud KD, Henderson WG, O’Dell JR. Shoulderarthroplasties have fewer complications than hip or knee arthroplasties in US vet-erans. Clin Orthop Relat Res. 2010 Mar;468(3):717-22. Epub 2009 Jul 21.92. Farshad M, Gerber C. Reverse total shoulder arthroplasty-from the most tothe least common complication. Int Orthop. 2010 Dec;34(8):1075-82. Epub 2010Sep 25.93. Seebauer L. Total reverse shoulder arthroplasty: European lessons and futuretrends. Am J Orthop (Belle Mead NJ). 2007 Dec;36(12)(Suppl 1):22-8.94. Wall B, Nove-Josserand L, O’Connor DP, Edwards TB, Walch G. Reverse totalshoulder arthroplasty: a review of results according to etiology. J Bone Joint Surg Am.2007 Jul;89(7):1476-85.95. Loehr J. Surgical management of the infected shoulder arthroplasty. In: CofieldRH, Sperling JW, editors. Revision and complex shoulder arthoplasty. Philadelphia:Lippincott Williams & Wilkins; 2010. p 214-23.96. Trampuz A, Zimmerli W. Prosthetic joint infections: update in diagnosis andtreatment. Swiss Med Wkly. 2005 Apr 30;135(17-18):243-51.97. Levy PY, Fenollar F, Stein A, Borrione F, Cohen E, Lebail B, Raoult D. Propioni-bacterium acnes postoperative shoulder arthritis: an emerging clinical entity. ClinInfect Dis. 2008 Jun 15;46(12):1884-6.98. Della Valle C, Bauer T, Malizos K. Workgroup 7: Diagnosis of periprosthetic jointinfection. In: Zmistowski B, editor. Proceedings of the international consensusmeeting on periprosthetic joint infection. Philadelphia; European Federation of Na-tional Associations of Orthopaedics and Traumatology; 2013. p 202-223.99. Patel A, Calfee RP, Plante M, Fischer SA, Green A. Propionibacterium acnescolonization of the human shoulder. J Shoulder Elbow Surg. 2009 Nov-Dec;18(6):897-902. Epub 2009 Apr 11.100. Athwal GS, Sperling JW, Rispoli DM, Cofield RH. Deep infection afterrotator cuff repair. J Shoulder Elbow Surg. 2007 May-Jun;16(3):306-11. Epub 2007Feb 22.101. Herrera MF, Bauer G, Reynolds F, Wilk RM, Bigliani LU, Levine WN. Infectionafter mini-open rotator cuff repair. J Shoulder Elbow Surg. 2002 Nov-Dec;11(6):605-8.

964

TH E J O U R N A L O F B O N E & JO I N T SU R G E RY d J B J S . O R G

VO LU M E 96-A d NU M B E R 11 d J U N E 4, 2014DI AG N O S I S A N D MA N AG E M E N T O F P E R I P R O S T H E T I C

SH O U L D E R IN F E C T I O N S

Page 10: Periprosthetic Shoulder Infections

102. Settecerri JJ, Pitner MA, Rock MG, Hanssen AD, Cofield RH. Infection afterrotator cuff repair. J Shoulder Elbow Surg. 1999 Jan-Feb;8(1):1-5.103. Bojar RA, Holland KT. Acne and Propionibacterium acnes. Clin Dermatol. 2004Sep-Oct;22(5):375-9.104. Fletcher RW, Fletcher SW. Clinical epidemiology, the essentials. 4th ed. Bal-timore: Williams & Wilkins; 2005. p 35-58.105. Bayston R, Nuradeen B, Ashraf W, Freeman BJ. Antibiotics for the eradicationof Propionibacterium acnes biofilms in surgical infection. J Antimicrob Chemother.2007 Dec;60(6):1298-301. Epub 2007 Oct 24.106. Holmberg A, Lood R, Morgelin M, Soderquist B, Holst E, Collin M, Christensson B,Rasmussen M. Biofilm formation by Propionibacterium acnes is a characteristic ofinvasive isolates. Clin Microbiol Infect. 2009 Aug;15(8):787-95. Epub 2009 Apr 23.107. Ramage G, Tunney MM, Patrick S, Gorman SP, Nixon JR. Formation of Propi-onibacterium acnes biofilms on orthopaedic biomaterials and their susceptibility toantimicrobials. Biomaterials. 2003 Aug;24(19):3221-7.108. Donlan RM. Biofilms and device-associated infections. Emerg Infect Dis. 2001Mar-Apr;7(2):277-81.109. Gristina AG, Costerton JW. Bacterial adherence to biomaterials and tissue.The significance of its role in clinical sepsis. J Bone Joint Surg Am. 1985Feb;67(2):264-73.110. Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR,Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R. Sonication ofremoved hip and knee prostheses for diagnosis of infection. N Engl J Med. 2007Aug 16;357(7):654-63.111. Kobayashi N, Bauer TW, Togawa D, Lieberman IH, Sakai H, Fujishiro T, Tuohy MJ,Procop GW. A molecular gram stain using broad range PCR and pyrosequencingtechnology: a potentially useful tool for diagnosing orthopaedic infections. Diagn MolPathol. 2005 Jun;14(2):83-9.112. Tunney MM, Patrick S, Curran MD, Ramage G, Hanna D, Nixon JR, Gorman SP,Davis RI, Anderson N. Detection of prosthetic hip infection at revision arthroplasty byimmunofluorescence microscopy and PCR amplification of the bacterial 16S rRNAgene. J Clin Microbiol. 1999 Oct;37(10):3281-90.113. Deirmengian C, Lonner JH, Booth RE Jr. The Mark Coventry Award: white bloodcell gene expression: a new approach toward the study and diagnosis of infection.Clin Orthop Relat Res. 2005 Nov;440:38-44.

114. Berbari E, Mabry T, Tsaras G, Spangehl M, Erwin PJ, Murad MH, Steckelberg J,Osmon D. Inflammatory blood laboratory levels as markers of prosthetic joint in-fection: a systematic review and meta-analysis. J Bone Joint Surg Am. 2010 Sep1;92(11):2102-9.115. Deirmengian C, Hallab N, Tarabishy A, Della Valle C, Jacobs JJ, Lonner J, BoothRE Jr. Synovial fluid biomarkers for periprosthetic infection. Clin Orthop Relat Res.2010 Aug;468(8):2017-23.116. Jacovides CL, Parvizi J, Adeli B, Jung KA. Molecular markers for diagnosis ofperiprosthetic joint infection. J Arthroplasty. 2011 Sep;26(6)(Suppl):99:e1. Epub2011 May 13.117. Parvizi J, Walinchus L, Adeli B. Molecular diagnostics in periprosthetic jointinfection. Int J Artif Organs. 2011 Sep;34(9):847-55.118. Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, Rizo-Rodrıguez JC,Little JW, Loyola-Rodrıguez JP. Detection of periodontal bacterial DNA in serum andsynovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol. 2009Dec;36(12):1004-10.119. Temoin S, Chakaki A, Askari A, El-Halaby A, Fitzgerald S, Marcus RE, Han YW,Bissada NF. Identification of oral bacterial DNA in synovial fluid of patients witharthritis with native and failed prosthetic joints. J Clin Rheumatol. 2012Apr;18(3):117-21.120. Gerard HC, Wang Z, Wang GF, El-Gabalawy H, Goldbach-Mansky R, Li Y,Majeed W, Zhang H, Ngai N, Hudson AP, Schumacher HR. Chromosomal DNA from avariety of bacterial species is present in synovial tissue from patients with variousforms of arthritis. Arthritis Rheum. 2001 Jul;44(7):1689-97.121. Parvizi J. Identification of Oral Bacterial DNA in Native and Failed ProstheticJoints. JBJS Orthop Highlights: Hip Surg. 2012;2(5):e6.122. Levy O, Iyer S, Atoun E, Peter N, Hous N, Cash D, Musa F, Narvani AA. Propi-onibacterium acnes: an underestimated etiology in the pathogenesis of osteoar-thritis? J Shoulder Elbow Surg. 2013 Apr;22(4):505-11. Epub 2012 Sep 13.123. Sankar WN, Esterhai JL. Sepsis of the shoulder girdle. In: Iannotti JP, WilliamsGR, editors. Disorders of the shoulder: diagnosis and management. Philadelphia:Lippincott Williams & Wilkins; 2007. p 1202-1231.124. Peel T, Buising K, Dowsey MM, Choong P. Management of prosthetic infectionaccording to organism. In: Kinov P, editor. Arthroplasty—Update. InTech; 2013. p517-535.

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