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Non-elective and revision arthroplasty are independently associated with hip and knee prosthetic joint infection caused by Acinetobacter baumannii: a Brazilian single center observational cohort study of 98 patients

Abstract

Background

Prosthetic joint infection (PJI) caused by Acinetobacter baumannii (Ab) has become a growing concern due to its overwhelming ability to express resistance to antibiotics and produce biofilm.

Aim

This study aimed to identify independent risk factors (RFs) associated with Ab-associated PJI and their role in the treatment outcome.

Methods

This was a single-centre, retrospective cohort study of PJI patients diagnosed between January 2014 and July 2018. A PJI diagnosis was made based upon the MSIS 2018 criteria. To estimate RFs associated with Ab-associated PJI, multivariate analyses with a level of significance of p < 0.05 were performed. To evaluate treatment failure, Kaplan–Meier analysis and log-rank test were performed.

Results

Overall, 98 PJI cases were assessed, including 33 with Ab-associated PJI and 65 with PJI involving other microorganisms (non–Ab-associated PJI). Independent RFs associated with Ab-associated PJI were revision arthroplasty [odds ratio (OR) = 3.01; 95% confidence interval (CI) = 1.15–7.90; p = 0.025] and nonelective arthroplasty (OR = 2.65; 95% CI = 1.01–7.01; p = 0.049). Ab-associated PJI was also more likely than non–Ab-associated PJI to be classified as a chronic late infection (OR = 5.81; 95% CI = 2.1–16.07; p = 0.001). Ab-associated PJI was not associated with treatment failure (p = 0.557).

Conclusions

Late chronic infections, surgical revision and nonelective arthroplasty are well-known predictors of PJI but were also independently associated with Ab-associated PJI. Infections caused by Ab and surgical treatment with debridement, antibiotics and implant retention were not associated with PJI treatment failure.

Trial registration

Study data supporting our results were registered with the Brazilian Registry of Clinical Trials (https://www.ensaiosclinicos.gov.br/rg/RBR-6ft5yb/), an open-access virtual platform for the registration of studies on humans performed in Brazil.

Registration no. RBR-6ft5yb.

Peer Review reports

Introduction

Worldwide, an increasing number of individuals have undergone joint-replacement surgeries, particularly at the hip and knee, either for elective reasons or following sustained trauma. Among all possible complications, prosthetic joint infection (PJI) is the one that is most feared; despite its low incidence, ranging from just 1 to 2% [1, 2] for primary and up to 4% for revision surgeries [3, 4], it boasts high morbidity and mortality rates. Gram-positive cocci (GPC), such as Staphylococcus aureus and coagulase-negative Staphylococci, are the major PJI-related microorganisms, followed by Gram-negative bacilli (GNB), with a prevalence ranging from 5 to 23% [4,5,6]. In some case series, PJIs attributed to GNB have been reported at rates greater than 40% [7, 8].

Acinetobacter is a genus of Gram-negative bacteria including a total of 31 different species. Due to its ability to spread in health care environments, Acinetobacter baumannii (Ab) is currently the most difficult species to control and eradicate [9]. This microorganism is ubiquitous in the environment [9] and has become one of the most successful pathogens associated with health care–related infections due to its ability to express a variety of antimicrobial resistance mechanisms and to form biofilms on both biotic and abiotic surfaces [10]. On a global scale, approximately 50% of Ab strains have been identified as multidrug-resistant (MDR). The World Health Organization (WHO) has declared carbapenem-resistant Ab in particular to be one of the most important species among Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Ab, Pseudomonas aeruginosa and Enterobacter sp.; these organisms are referred to collectively as the ESKAPE group and are considered priority pathogens due to the threat they pose to global public health, necessitating urgent actions and the development of new antibiotics to combat them [11, 12]. Unfortunately, in several Latin American countries, Ab strains have shown resistance to virtually all classes of antibiotics, including carbapenems. This worrisome microbial epidemiology has been identified at some Brazilian hospitals, where 77% of these isolates have exhibited resistance to carbapenems [13]. The production of oxacillin-hydrolysing carbapenemase (carbapenem-hydrolysing class D enzymes) has been identified as the most common antibiotic resistance mechanism, and the global dissemination of OXA-type clones, including OXA-23, OXA-72 and OXA-58, is regarded as the most common mechanism of antibiotic resistance [13, 14].

The emergence of musculoskeletal surgical site infections and orthopaedic implant–associated infections caused by Ab has become a matter of urgent concern for health care providers due to the limited therapeutic arsenal available, particularly against carbapenem-resistant strains [15]. Moreover, the treatment of PJIs caused by MDR and extensively drug-resistant (XDR) GNB, particularly Ab, is hampered by its ability to be encased within biofilms. The resistance of Ab against virtually all antimicrobials and its intrinsic capacity for biofilm formation may correlate with lower cure rates and increased disease morbidity since treatment usually requires a combination of highly toxic systemic antibiotics [16, 17]. Despite this challenge, to our knowledge, no published studies have investigated independent risk factors (RFs) for Ab-associated PJI. Indeed, few previous publications on Ab-associated PJI have attempted to describe, in a case series report format, aspects of surgical and antibiotic therapy [15, 18, 19]. Therefore, this study aimed to identify the independent RFs for Ab-associated PJI and to assess the role of Ab in treatment outcome.

Materials and methods

Study design

This study was performed as an observational, single-centre, retrospective, cohort study using data obtained from 2672 patients undergoing arthroplasties between January 2014 and July 2018, at a Brazilian orthopaedic referral centre. All patients diagnosed with PJI, either due to Ab (Ab-PJI) and other microorganisms (Non-Ab-PJI), were identified from clinical and microbiological records and surgical description sheets. The primary study endpoint was the identification of independent predisposing factors associated with PJI caused by Ab and secondary endpoint was to access if the Ab-PJI have influence on treatment outcome. The study included individuals aged 18 years or older who met the diagnosis criteria for PJI according to the Musculoskeletal Infection Society (MSIS) [20]. Inclusion criteria also required the same identified pathogen yielding in at least two peri-prosthetic tissue samples, and prospective follow-up period of a minimum one-year period. Patients who underwent arthroplasty at an institution other than ours, did not meet the criteria for PJI as defined by the MSIS or had culture-negative results were excluded. The study was reviewed and approved by the local ethics committee (approval no. 2,610,914 on April 20, 2018).

Definitions

The PJI onset date was defined according to the date of the first observation of typical infectious signs and symptoms. MDR- Ab was defined as the nonsusceptibility of the identified pathogen to at least one antimicrobial agent from three or more different antimicrobial classes (e.g., aminoglycosides, cephalosporins with an anti-Pseudomonas effect, carbapenems, fluoroquinolones, penicillin + β-lactamase inhibitors, monobactams and polymyxin). Ab that were extensively drug-resistant (XDR) to multiple antibiotics were defined as those lacking susceptibility to at least one antimicrobial agent from all but two classes of antimicrobials [21].

Early-onset PJI was defined as those cases occurring < 3 months after the index surgery, whereas late PJI was defined as those cases in which the diagnosis occurred more than 3 months after the index surgery. The remission of infection was defined as the absence of clinical, laboratory, or radiological symptoms at the last medical follow-up (with a minimum follow-up time of 1 y). Therapeutic failure was defined as infection recurrence at a previously controlled site; requirement for new surgery, a second course of antimicrobial therapy, chronic antibiotic suppression, excision arthroplasty, or limb amputation; or death within the follow-up period [22, 23].

Microbiological analysis

In the surgical ward, a minimal of three different periprosthetic tissue samples and synovial fluid were collected and processed for microbiology. Synovial fluid sample were aseptically inoculated into aerobic standard blood culture bottles. Tissue samples were homogenised in 3 ml of brain-heart infusion (BHI) broth for 1 min and inoculated onto aerobic sheep blood agar, chocolate agar, and anaerobic blood agar and into thioglycolate broth (BD Diagnostic Systems, Sparks, MD). The time limit for processing samples was 6 h. Aerobic were incubated aerobically at 35–37 °C in 5–7% CO2 for 7 days, and anaerobic plates were incubated at 37 °C for 14 days. Additionally, 0.5 ml of tissue homogenate was inoculated in thioglycolate broth, incubated for 14 days, and sub-cultured on blood agar plates when the broth became cloudy. Colonies of microorganisms growing on plates were identified, and their susceptibilities to antibiotics were tested according to standard microbiological techniques. The bacteria were identified by conventional biochemical and metabolic tests in accordance with the international standards and definitions established by the European Committee on Antimicrobial Susceptibility Testing (EUCAST) [24]. Sensitivity tests were performed using the disk diffusion technique, and the determination of minimum inhibitory concentrations (MICs) was performed by automated means or by the e-test method, the results of which are presented according to standardised microbiological techniques.

Potential risk factors

Variables associated with the patient, surgery, and postoperative procedures were identified by reviewing the medical, intraoperative, and microbiological records to identify potential RFs for Ab-PJI. Demographic variables (sex and age), comorbidities (the presence and number of comorbidities, alcoholism, and smoking habits), the American Society of Anaesthesiologists (ASA) physical status classification, previous use of antibiotics during the past 3 m, and previous orthopaedic infections were assessed. Associated surgical aspects included the arthroplasty site (hip vs knee), total or partial arthroplasty, primary or revision surgery, and post-traumatic arthroplasty or elective arthroplasty. The factors related to the postoperative period that were considered included postoperative hematoma, the presence of sepsis at the time of diagnosis, concomitant infections diagnosed at different sites, and early or late infection. The surgical strategies, including debridement, antibiotics, and implant retention (DAIR) or any prosthesis removal (Non-DAIR), were assessed for survival and outcome analyses.

Statistical analysis

For the overall study population and the groups defined as Ab-PJI and Non-Ab-PJI, qualitative variables are reported as the mean and percentage, and quantitative variables are presented as the median and standard deviation (SD). Associations between qualitative variables were analysed using the Chi-square test and Fisher’s exact test, as indicated. The associations between quantitative variables were assessed by logistic regression. The risk estimate was calculated for the associated variables and reported as the odds ratio (OR) with a 95% confidence interval (CI). The logistic regression model was used to select significant variables from among those identified as significant in univariate analyses. Only variables with significance less than 0.20 (p < 0.20) were included in the logistic regression. Variables with significance less than 0.05 (p < 0.05) in the multiple regression were included in the final model. To estimate the probability of survival as a function of time, Kaplan-Meier (KM) analyses were performed, and the resulting curves were compared using the log-rank method. All data were analysed using SPSS, version 23 (IBM-SPSS Inc., Chicago, IL, USA).

Results

A total of 115 PJI cases were assessed for inclusion in the study; of these, 14 cases that did not meet the MSIS criteria for infection and three cases with less than two or with negative tissue cultures were excluded. Therefore, 98 PJI cases were finally analysed, including 33 in the Ab-associated PJI group and 65 in the non–Ab-associated PJI group.

Study population

The demographic and clinical characteristics of the study population are summarised in Additional file 1. Most PJI patients were women (58.16%), with a mean ± standard deviation age of 67.3 ± 13.2 years. Interestingly, hip arthroplasty was the most frequent procedure (83.7%). More than 70% of patients had at least one comorbidity, with hypertension (61.2%) and diabetes mellitus (20.4%) being the most common. Arthroplasty was the primary surgery in 57.1% (56/98) of cases and was performed to address a fracture (nonelective) in 39.8% (39/98). PJI was classified as early in 69.4% (68/98), and 19.4% (19/98) of patients had experienced a PJI previously (Additional file 1).

Microbiology

Among 33 patients with Ab-associated PJI, 27 strains were classified as XDR strains, four were classified as MDR strains and two strains were sensitive to multiple antibiotics. Although the rate of susceptibility to carbapenem was below 6%, all isolates were 100% susceptible to colistin (Table 1).

Table 1 Antibiotic susceptibility of Ab strains

Culture yields in the non–Ab-associated PJI group were mainly S. aureus, Enterobacter aerogenes and P. aeruginosa. The rate of methicillin-resistant S. aureus identification was 7.0% (Additional file 2).

Outcomes and potential risk factors for ab-associated PJI

During the univariate analysis, RFs associated with patient characteristics, surgery and the postoperative period were investigated for possible associations with Ab-associated PJI, as shown in Table 2. As compared with PJIs caused by other microorganisms, Ab-associated PJI was significantly associated with previous antibiotics usage in the last three months (51.5% vs 30.8%; p = 0.045), previous orthopaedic infections (36.4% vs 12.3%; p = 0.005), revision arthroplasty (60.6% vs 33.8%; p = 0.011) and posttraumatic/nonelective arthroplasty (54.4% vs 32.3%; p = 0.034). Eighteen patients in the Ab-associated PJI group underwent nonelective arthroplasty for reasons such as high-energy trauma (n = 4) and falling from a height while elderly (n = 14). Patients with Ab-associated PJIs received more blood transfusions than those with PJIs caused by other microorganisms (36.4% vs 10.8%; p = 0.002). Early infections occurred in 48.5% (16/33) of patients with Ab-associated PJIs and 81.5% (53/65) of patients with non–Ab-associated PJIs (p = 0.001), respectively. Following an infectious diagnosis, DAIR was the surgical strategy chosen for 57.6% of the Ab-associated PJI cases (p = 0.047) (Table 2). The factors that remained independently associated with Ab-associated PJI following multiple logistic regression were revision arthroplasty [odds ratio (OR) = 3.01; 95% confidence interval (CI) = 1.15–7.90; p = 0.025] and nonelective arthroplasty (OR = 2.65; 95% CI = 1.01–7.01; p = 0.049). In addition, Ab-associated PJIs were more likely than non–Ab-associated PJIs to be classified as late chronic infections (OR = 5.81; 95% CI = 2.1–16.07; p = 0.001) (Table 3).

Table 2 Univariate analysis of risk factors associated with Ab-PJIa
Table 3 Predisposing factors independently associated to Acinetobacter baumannii PJI –multivariate analysis

On the Kaplan–Meier survival curve, infection by Ab was not identified as an RF for treatment failure (p = 0.557) (Fig. 1), and no increase in the failure rate was observed for the Ab-associated PJI group that underwent DAIR in comparison with the non–Ab-associated PJI group that underwent DAIR (p = 0.530) (Fig. 2).

Fig. 1
figure 1

Kaplan–Meier survival curve for death/recurrence considering PJIs caused by Ab-PJI

Fig. 2
figure 2

Kaplan-Meir survival curve for death/recurrence considerung PJI by A. buamannii PJI DAIR versus Non-Ab-PJI DAIR

Discussion

To our knowledge, this is the first study to investigate predisposing factors associated with Ab-associated PJI. Interestingly the well-known predictors of PJI – which include revision surgeries, nonelective arthroplasties and late infections (PJI diagnosed after 3 m of index surgery) – were independently associated with Ab infection. This likely reflects the particular epidemiology of a Brazilian orthopaedic referral centre, where the rates of nosocomial SSI caused by MDR-GNB are high [25, 26]. In addition, the high selective pressure imposed by misuse of empirical broad-spectrum antibiotics is likely to have played a major role [27]. Since then, a local antimicrobial stewardship program has been implemented as a tool to enhance the appropriateness of antibiotics prescriptions.

In the microbiological sample, a greater frequency (81.8%) of Ab strains causing PJI were XDR strains, whereas 12.1% were MDR strains and only 6.1% were sensitive to multiple antibiotics. The rate of susceptibility to carbapenems was worryingly low, with only 3% of cases sensitive to imipenem and only 6% sensitive to meropenem. The higher prevalence of Ab-associated PJI at our institution was not assumed to represent an outbreak but instead an endemic nosocomial pathogen typically identified in the intensive care unit environment that boasts an overwhelming ability to colonise the human skin. Furthermore, before 2018, immediate postoperative care protocols for patients who undergo arthroplasty in our hospital were usually enacted in the intensive care unit, which is likely to have increased the rate of skin colonisation by Ab strains.

Orthopaedic implant–associated infections have traditionally been considered difficult to treat due to the formation of bacterial biofilms on the implant surface and the low levels of antibiotic penetration into bone tissue and biofilms [28, 29]. In addition, the higher levels of bacterial resistance commonly expressed by Ab makes treatment of infections involving this organism even more challenging due to the scarcity of available drugs and the potential for antibiotic-related toxicity [30]. Although Ab is ubiquitous in nature and colonises the skin of healthy individuals, most human infections by this organism are health care–associated. A systematic review by Falagas et al. [31], which included 55 articles describing Ab infections, linked Ab infections to prolonged hospital stays, intensive care unit treatments and the use of invasive devices.

Despite the poor availability of studies specifically describing Ab-associated PJI, the number of osteomyelitis and fracture-related infections caused by Ab seems to be on the rise worldwide, especially when considering those associated with high-kinetic energy trauma and open fractures [32]. Many studies have described a strong association between complex traumatic gunshot wounds resulting in fracture-related infections or osteomyelitis and Ab infection in various conflict-affected regions, such as Iraq, Afghanistan and Yemen [3235]. However, whether Ab is acquired during the act of injury itself from primary contamination or is acquired in the hospital during the trauma care and subsequent surgical procedures remains unclear. In addition to reports from Middle Eastern countries, a study by Vanegas et al. [36] from Colombia addressed osteomyelitis, skin and soft tissue infections and reported an increased number of infections caused by Ab, with a strong association with recent hospitalisation or surgery and previous use of antimicrobials in the past 6 m. Despite the increased risk of PJI following revision surgery [37,38,39], the association between revision arthroplasty and Ab-associated PJI has not yet been explored in the literature. However, we are aware that implant contamination during surgery is a primary source of infection, and patients previously colonised with Ab may be at increased risk for PJI.

In our study, a 2.6-fold increase in the risk of Ab-associated PJI was identified among patients undergoing an emergency arthroplasty, which suggests that, similar to in the case of fracture-related infections, posttraumatic arthroplasty may be a factor that predisposes patients to Ab-associated PJI. The reasons underlying the association between trauma and Ab infection were not elucidated in this study and require further investigation. In addition, we were unable to identify any independent associations between Ab-associated PJI and closed proximal femoral fractures in the elderly population, recent hospitalisation history or recent use of antibiotics. However, nonelective arthroplasties may necessitate longer preoperative hospital stays due to the mandatory propaedeutic for assessing preoperative risks and the need to compensate for clinical comorbidities prior to performing the surgical procedure, which might increase the risk of colonisation by Ab [40]. However, the length of preoperative hospital stay, which could validate this hypothesis, was not a variable that was assessed in the present study.

In our study, late PJI was independently associated with Ab infection, and a possible explanation may rely upon the lower level of virulence expression when bacteria express multiple antibiotic-resistant mechanisms. Several mechanisms associated with antimicrobial resistance, including pump efflux and biofilm organisation abilities, also reduce the bacterial replicative capacity [41]. This stationary phase, associated with biofilm formation and maturation, is likely to cause Ab infections to develop more slowly, increasing the likelihood of being diagnosed as late PJI [42, 43]. Neither Ab infection nor the surgical strategy used after the infectious diagnosis was independently associated with the final outcome or the risk of treatment failure. Few studies to date have assessed the prognostic factors associated with Ab-associated PJI development, although some have reported high rates of therapeutic failure in Ab-associated PJIs; for example, Vasso et al. [19] described a 33.3% failure rate for the treatment of Ab-associated PJI. However, their study was underpowered, assessing only nine patients in a group containing a mix of infections associated with both Ab and P. aeruginosa. Another study that assessed the outcomes of PJI caused by GNB -MDR reported that infections caused by MDR/XDR GNB were associated with high therapeutic failure rates when DAIR (52.2%) was performed as compared to when non-DAIR treatment strategies were employed (23.4%) [44]. However, only three patients had Ab-associated PJIs in this previous study, which is not a representative sample.

Importantly, the present study has potential limitations. First, it was performed as a retrospective investigation and took place at a single centre located in a major city in a developing country offering specialised orthopaedic care for the regional population. Consequently, the results obtained at our hospital may not apply to other hospitals. In addition, the identification and sensitivity tests were performed using nonautomated methods, and no molecular or genotypic analyses were performed to identify clonal variants or similar patterns of resistance mechanisms. Furthermore, no pairing was performed between the Ab-associated PJI and non–Ab-associated PJI groups to control for preoperative hospitalisation times or preoperative colonisation by Ab, which could support the hypothesis that PJI contamination occurred intraoperatively. However, this study explored the previously unexamined issue of PJI-predisposing factors and relied on the largest number of Ab infection cases described to date, with a high frequency of MDR/ XDR strains.

Conclusions

The findings suggest that nonelective and revision arthroplasties primarily performed due to trauma and PJI diagnosed three months after the index surgery were independently associated with Ab-associated PJI. In addition, PJI caused by Ab was not associated with treatment failure, and no difference according to DAIR in the Ab-associated PJI versus non–Ab PJI groups was identified for the disease-free survival rate. The present study adds relevant data to the growing field of MDR-GNB PJI cases, but larger, multicentre cohort studies are still needed.

Availability of data and materials

Study data supporting our results were registered at an open access virtual platform for registration of studies on humans performed in Brazil. The Brazilian Registry of Clinical Trials (ReBEC) http://www.ensaiosclinicos.gov.br/rg/RBR-6ft5yb/

Register Number: RBR-6ft5yb.

Abbreviations

Ab :

Acinetobacter baumannii

ASA:

American Society of Anesthesiologists

BHI:

Brain-heart infusion

CI:

Confidence interval

DAIR:

(Debridement, antibiotics, and implant retention)

EUCAST:

European Committee on Antimicrobial Susceptibility Testing

GNB:

Gram-negative bacilli

GPC:

Gram-positive cocci

ICU:

Intensive care unit

KM:

Kaplan–Meier

OR:

Odds ratio

OXA:

Oxacillin-hydrolysing

MRSA:

Methicillin-resistant Staphylococcus aureus

MIC:

Minimum inhibitory concentrations

MDR:

Multidrug-resistant

MSIS:

Musculoskeletal Infection Society

PJI:

Prosthetic joint infection

RF:

Risk factors

SD:

Standard deviation

SSI:

Surgical site infections

WHO:

World Health Organization

XDR:

Extensively drug-resistant

References

  1. Kozak LJ, DeFrances CJ, Hall MJ. National hospital discharge survey: 2004 annual summary with detailed diagnosis and procedure data. Vital Health Stat 13. 2006; (162): 1–209. PMID: 17091747

  2. Corvec S, Portillo ME, Pasticci BM, Borens O, Trampuz A. Epidemiology and new developments in the diagnosis of prosthetic joint infection. Int J Artif Organs 2012; 35(10):923–934. doi: https://doi.org/10.5301/ijao.5000168. PMID: 23138706.

  3. Ong KL, Kurtz SM, Lau E, Bozic KJ, Berry DJ, Parvizi J. Prosthetic joint infection risk after total hip arthroplasty in the Medicare population. J Arthroplast 2009; 24(6 Suppl):105–109. doi: https://doi.org/10.1016/j.arth.2009.04.027. Epub 2009 Jun 2. PMID: 19493644.

  4. Martínez-Pastor JC, Muñoz-Mahamud E, Vilchez F, García-Ramiro S, Bori G, Sierra J, Martínez JA, Font L, Mensa J, Soriano A. Outcome of acute prosthetic joint infections due to gram-negative bacilli treated with open debridement and retention of the prosthesis. Antimicrob Agents Chemother. 2009; 53(11): 4772–4777. doi: https://doi.org/10.1128/AAC.00188-09. Epub 2009 Aug 17. PMID: 19687237; PMCID: PMC2772308.

  5. Hsieh PH, Lee MS, Hsu KY, Chang YH, Shih HN, Ueng SW. Gram-negative prosthetic joint infections: risk factors and outcome of treatment. Clin Infect Dis 2009;49(7):1036–1043. doi: https://doi.org/10.1086/605593. PMID: 19691430.

  6. Zimmerli W, Trampuz A, Ochsner PE. Prosthetic-joint infections. N Engl J Med 2004; 351(16):1645–1654. doi: https://doi.org/10.1056/NEJMra040181. PMID: 15483283.

  7. Pradella JGDP, Bovo M, Salles MJC, Klautau GB, Camargo OAP, Cury RPL. Infected primary knee arthroplasty: Risk factors for surgical treatment failure. Rev Bras Ortop. 2013; 48(5): 432–437. doi: https://doi.org/10.1016/j.rboe.2012.10.006. PMID: 31304148; PMCID: PMC6565953.

  8. Nagaya LH, Salles MJC, Takikawa LSC, Fregoneze M, Doneux P, Silva LAD, Sella GDV, Miyazaki AN, Checchia SL. Infections after shoulder arthroplasty are correlated with higher anesthetic risk score: a case-control study in Brazil. Braz J Infect Dis 2017; 21(6):613–619. doi: https://doi.org/10.1016/j.bjid.2017.06.003. Epub 2017 Jul 10. PMID: 28704642.

  9. Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev. 2008; 21(3): 538–582. doi: https://doi.org/10.1128/CMR.00058-07. PMID: 18625687; PMCID: PMC2493088.

  10. Longo F, Vuotto C, Donelli G. Biofilm formation in Acinetobacter baumannii. New Microbiol 2014; 37(2):119–127. Epub 2014 Apr 1. PMID: 24858639.

  11. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 2009; 48(1):1–12. doi: https://doi.org/10.1086/595011. PMID: 19035777

  12. CDC. Antibiotic resistance Threats in the United States 2019. Atlanta: U.S. Department of Health and Human Services, CDC; 2019.

    Google Scholar 

  13. Labarca JA, Salles MJ, Seas C, Guzmán-Blanco M. Carbapenem resistance in Pseudomonas aeruginosa and Acinetobacter baumannii in the nosocomial setting in Latin America. Crit Rev Microbiol 2016;42(2):276–292. doi: https://doi.org/10.3109/1040841X.2014.940494. Epub 2014 Aug 27. PMID: 25159043.

  14. Escandón-Vargas K, Reyes S, Gutiérrez S, Villegas MV. The epidemiology of carbapenemases in Latin America and the Caribbean. Expert Rev Anti-Infect Ther 2017 Mar;15(3):277–297. doi: https://doi.org/10.1080/14787210.2017.1268918. Epub 2016 Dec 20. PMID: 27915487.

  15. Hischebeth GT, Wimmer MD, Molitor E, Seifert H, Gravius S, Bekeredjian-Ding I. Multidrug resistant Acinetobacter baumannii reaches a new frontier: prosthetic hip joint infection. Infection. 2015; 43(1):95–97. doi: https://doi.org/10.1007/s15010-014-0661-x. Epub 2014 Jul 19. PMID: 25037735.

  16. Krzyściak P, Chmielarczyk A, Pobiega M, Romaniszyn D, Wójkowska-Mach J. Acinetobacter baumannii isolated from hospital-acquired infection: biofilm production and drug susceptibility. APMIS. 2017; 125(11):1017–1026. doi: https://doi.org/10.1111/apm.12739. Epub 2017 Sep 15. PMID: 28913903.

  17. Runci F, Bonchi C, Frangipani E, Visaggio D, Visca P. Acinetobacter baumannii Biofilm Formation in Human Serum and Disruption by Gallium. Antimicrob Agents Chemother. 2016; 61(1): e01563–e01516. doi: https://doi.org/10.1128/AAC.01563-16. PMID: 27799219; PMCID: PMC5192145.

  18. Vila A, Pagella H, Amadio C, Leiva A. Acinetobacter Prosthetic Joint Infection Treated with Debridement and High-Dose Tigecycline. Infect Chemother. 2016; 48(4): 324–329. doi: https://doi.org/10.3947/ic.2016.48.4.324. Epub 2016 Nov 8. PMID: 27883369; PMCID: PMC5204012.

  19. Vasso M, Schiavone Panni A, De Martino I, Gasparini G. Prosthetic knee infection by resistant bacteria: the worst-case scenario. Knee Surg Sports Traumatol Arthrosc 2016; 24(10):3140–3146. doi: https://doi.org/10.1007/s00167-016-4010-8. Epub 2016 Feb 1. PMID: 26831859.

  20. Parvizi J, Zmistowski B, Berbari EF, Bauer TW, Springer BD, Della Valle CJ, Garvin KL, Mont MA, Wongworawat MD, Zalavras CG. New definition for periprosthetic joint infection: from the Workgroup of the Musculoskeletal Infection Society. Clin Orthop Relat Res. 2011; 469(11): 2992–2994. doi: https://doi.org/10.1007/s11999-011-2102-9. PMID: 21938532; PMCID: PMC3183178.

  21. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012; 18(3): 268-281. doi: https://doi.org/10.1111/j.1469-0691.2011.03570.x. Epub 2011 Jul 27. PMID: 21793988.

  22. Kandel CE, Jenkinson R, Daneman N, Backstein D, Hansen BE, Muller MP, Katz KC, Widdifield J, Bogoch E, Ward S, Sajja A, Jeldes FG, McGeer A. Predictors of Treatment Failure for Hip and Knee Prosthetic Joint Infections in the Setting of 1- and 2-Stage Exchange Arthroplasty: A Multicenter Retrospective Cohort. Open Forum Infect Dis. 2019; 6(11): ofz452. doi: https://doi.org/10.1093/ofid/ofz452. PMID: 31737739; PMCID: PMC6847009.

  23. Shohat N, Goswami K, Tan TL, Fillingham Y, Parvizi J. Increased failure after irrigation and debridement for acute Hematogenous Periprosthetic joint infection. J Bone Joint Surg Am 2019; 101(8):696–703. doi: https://doi.org/10.2106/JBJS.18.00381. PMID: 30994587.

  24. Eclercq R, Cantón R, Brown DF, Giske CG, Heisig P, MacGowan AP, Mouton JW, Nordmann P, Rodloff AC, Rossolini GM, Soussy CJ, Steinbakk M, Winstanley TG, Kahlmeter G. EUCAST expert rules in antimicrobial susceptibility testing. Clin Microbiol Infect 2013;19(2):141–160. doi: https://doi.org/10.1111/j.1469-0691.2011.03703x. Epub 2011 Nov 25. PMID: 22117544.

  25. Villegas MV, Blanco MG, Sifuentes-Osornio J, Rossi F. Increasing prevalence of extended-spectrum-beta-lactamase among gram-negative bacilli in Latin America--2008 update from the study for monitoring antimicrobial resistance trends (SMART). Braz J Infect Dis 2011; 15(1):34–39. PMID: 21412587.

  26. Gales AC, Castanheira M, Jones RN, Sader HS. Antimicrobial resistance among gram-negative bacilli isolated from Latin America: results from SENTRY antimicrobial surveillance program (Latin America, 2008-2010). Diagn Microbiol Infect Dis 2012;73(4):354–360. doi: https://doi.org/10.1016/j.diagmicrobio.2012.04.007. Epub 2012 May 31. PMID: 22656912.

  27. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010; 74(3): 417–433. doi: https://doi.org/10.1128/MMBR.00016-10. PMID: 20805405; PMCID: PMC2937522.

  28. del Pozo JL, Patel R. The challenge of treating biofilm-associated bacterial infections. Clin Pharmacol Ther 2007; 82(2):204–209. doi: https://doi.org/10.1038/sj.clpt.6100247. Epub 2007 May 30. PMID: 17538551.

  29. Saunders RK Jr, Infanti J, Ali H, Shuey T, Potteiger C, McNeilly S, Adams CS. Gram-negative Bacteria are internalized into osteocyte-like cells. J Orthop Res 2020; 38(4):861–870. doi: https://doi.org/10.1002/jor.24510. Epub 2019 Nov 17. PMID: 31692074.

  30. Siljander MP, Sobh AH, Baker KC, Baker EA, Kaplan LM. Multidrug-resistant organisms in the setting of Periprosthetic joint infection-diagnosis, prevention, and treatment. J Arthroplast 2018; 33(1):185–194. doi: https://doi.org/10.1016/j.arth.2017.07.045. Epub 2017 Aug 3. PMID: 28869114.

  31. Falagas ME, Kopterides P. Risk factors for the isolation of multi-drug-resistant Acinetobacter baumannii and Pseudomonas aeruginosa: a systematic review of the literature. J Hosp Infect 2006;64(1):7–15. doi: https://doi.org/10.1016/j.jhin.2006.04.015. Epub 2006 Jul 5. PMID: 16822583.

  32. Schafer JJ, Mangino JE. Multidrug-resistant Acinetobacter baumannii osteomyelitis from Iraq. Emerg Infect Dis. 2008; 14(3): 512–514. doi: https://doi.org/10.3201/eid1403.070128. PMID: 18325278; PMCID: PMC2570836.

  33. Murphy RA, Ronat JB, Fakhri RM, Herard P, Blackwell N, Abgrall S, Anderson DJ. Multidrug-resistant chronic osteomyelitis complicating war injury in Iraqi civilians. J Trauma 2011; 71(1):252–254. doi: https://doi.org/10.1097/TA.0b013e31821b8622. PMID: 21818032.

  34. Yun HC, Branstetter JG, Murray CK. Osteomyelitis in military personnel wounded in Iraq and Afghanistan. J Trauma. 2008; 64(2 Suppl): S163–S168; discussion S168. doi: https://doi.org/10.1097/TA.0b013e318160868c. PMID: 18376160.

  35. Lohr B, Pfeifer Y, Heudorf U, Rangger C, Norris DE, Hunfeld KP. High prevalence of multidrug-resistant Bacteria in Libyan war casualties admitted to a tertiary care hospital, Germany. Microb Drug Resist 2018; 24(5):578–584. doi: https://doi.org/10.1089/mdr.2017.0141. Epub 2017 Oct 17. PMID: 29039717.

  36. Vanegas JM, Higuita LF, Vargas CA, Cienfuegos AV, Rodríguez ÉA, Roncancio GE, Jiménez JN. Acinetobacter baumannii resistente a carbapenémicos causante de osteomielitis e infecciones de la piel y los tejidos blandos en hospitales de Medellín, Colombia [Carbapenem-resistant Acinetobacter baumannii causing osteomyelitis and infections of skin and soft tissues in hospitals of Medellín, Colombia]. Biomedica. 2015; 35(4): 522–530. Spanish. doi: https://doi.org/10.7705/biomedica.v35i4.2572. PMID: 26844441.

  37. Jacobs AME, Bénard M, Meis JF, van Hellemondt G, Goosen JHM. The unsuspected prosthetic joint infection: incidence and consequences of positive intra-operative cultures in presumed aseptic knee and hip revisions. Bone Joint J 2017; 99-B(11):1482–1489. doi: https://doi.org/10.1302/0301-620X.99B11.BJJ-2016-0655.R2. PMID: 29092987.

  38. Hoell S, Moeller A, Gosheger G, Hardes J, Dieckmann R, Schulz D. Two-stage revision arthroplasty for periprosthetic joint infections: what is the value of cultures and white cell count in synovial fluid and CRP in serum before second stage reimplantation? Arch Orthop Trauma Surg 2016; 136(4):447–452. doi: https://doi.org/10.1007/s00402-015-2404-6. Epub 2016 Jan 12. PMID: 26757939.

  39. Kunutsor SK, Whitehouse MR, Blom AW, Beswick AD; INFORM Team. Patient-Related Risk Factors for Periprosthetic Joint Infection after Total Joint Arthroplasty: A Systematic Review and Meta-Analysis. PLoS One. 2016; 11(3): e0150866. doi: https://doi.org/10.1371/journal.pone.0150866. PMID: 26938768; PMCID: PMC4777569.

  40. Thorne A, Luo T, Durairajan NK, Kaye KS, Foxman B. Risk factors for endemic Acinetobacter Baumannii colonization: A case-case study. Am J Infect Control. 2019; 47(11):1294–1297. doi: https://doi.org/10.1016/j.ajic.2019.04.179. Epub 2019 Jun 26. PMID: 31253551).

  41. Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJ. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol. 2015; 13(1): 42–51. doi: https://doi.org/10.1038/nrmicro3380. Epub 2014 Dec 1. PMID: 25435309).

  42. Salles MJ, Zurita J, Mejía C, Villegas MV; Latin America Working Group on Bacterial Resistance. Resistant gram-negative infections in the outpatient setting in Latin America. Epidemiol Infect. 2013; 141(12): 2459–2472. doi: https://doi.org/10.1017/S095026881300191X. Epub 2013 Aug 7. PMID: 23924513; PMCID: PMC3821403.

  43. Dai J, Jiang C, Chen H, Chai Y. Assessment of the risk factors of multidrug-resistant organism infection in adults with type 1 or type 2 diabetes and diabetic foot ulcer. Can J Diabetes 2020; 44(4):342–349. doi: https://doi.org/10.1016/j.jcjd.2019.10.009. Epub 2019 Nov 9. PMID: 32005564.

  44. Papadopoulos A, Ribera A, Mavrogenis AF, Rodriguez-Pardo D, Bonnet E, José Salles M, et al. Corrigendum to "Multidrug-resistant and extensively drug-resistant Gram-negative prosthetic joint infections: Role of surgery and impact of colistin administration" [International Journal of Antimicrobial Agents 53(3) (2019) 294–301]. Int J Antimicrob Agents. 2019;53(4):538–9 https://doi.org/10.1016/j.ijantimicag.2019.03.005. Epub 2019 Mar 23. Erratum for: Int J Antimicrob Agents. 2019 Mar;53(3):294–301. PMID: 30910479.

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Acknowledgements

We would like to thank the” Fundação Hospitalar São Francisco de Assis” for the support to conduct this study.

Informed consent statement

Informed Consent Statement was waived by ethics committee of of Fundação Hospitalar São Francisco de Assis.

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This research received no external funding.

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Authors and Affiliations

Authors

Contributions

Conceptualization, RBS. and MJCS.; methodology, RBS. and MJCS; validation, MJCS., formal analysis, MJCS.; investigation RBS and ROA.; data curation, RBS.; writing—original draft preparation, RBS and MJCS.; writing—review and editing, MJCS and ROA; visualization, MJCS.; supervision, MJCS.; project administration, RBS. All authors have read and agreed to the published version of the manuscript.

Authors’ information

Raquel Bandeira da Silva: Graduated in medicine at the Federal University of Minas Gerais (UFMG) (2007–2012). Specialized in infectious diseases by the Instituto de Infectologia Emilio Ribas (IIER-SP) (2013–2016). She is working towards a PhD in health sciences from the Faculty of Medicine of Santa Casa de São Paulo (2018 - until now).

Corresponding author

Correspondence to Mauro José Salles.

Ethics declarations

Ethics approval and consent to participate

The study was conducted according to the guidelines of the Declaration of Helsinki and approved by Ethics Committee) of Fundação Hospitalar São Francisco de Assis (no. 2,610,914 on April 20, 2018).

Consent for publication

Not applicable.

Competing interests

The authors declare no conflict of interest.

Rodrigo Otavio Dias de Araújo: Specialist doctor in Orthopedics, Traumatology and Sports Medicine. Master’s in health education. Technical Director and Principal Investigator of Fundação Hospitalar São Francisco de Assis - Santa Lúcia Unit. Head of Orthopedics. University Professor at the José do Rosário Vellano University (UNIFENAS). Professor of the Medicine course and coordinator of the Post-Graduation in Health Education at the Faculty of Medical Sciences of Minas Gerais (FCM / FELUMA-MG).

Mauro Costa Salles: Graduated in Medicine at Federal University of Pará (State of Pará) (1983–1988), Specialization in Internal Medicine at” Santa Casa de Misericórdia de São Paulo “(1989-1991) and Medical Residency in Infectious Diseases at the “Instituto de Infectologia Emílio Ribas” (1993–1995).Attended the Master of Science (MSc) in Applied Molecular Biology of Infectious Diseases by the London School of Hygiene & amp; Tropical Medicine (LSHTM), University of London-UK (1998). Doctorate obtained in 2008 by the Faculty of Medical Sciences of Santa Casa de São Paulo. He is currently an Adjunct Professor of the Discipline of Infectious Diseases at the Faculty of Medical Sciences of Santa Casa de São Paulo (FCMSCSP) and Coordinator of the Infectious Diseases Clinic at the “Irmandade da Santa Casa de Misericórdia de São Paulo” (FCMSCSP). Member of the Board of the Postgraduate Program in Health Sciences at FCMSCSP since 2017.Since 2018 he has also been Adjunct Professor A1 of the Discipline of Infectious and Parasitic Diseases at the Federal University of São Paulo (UNIFESP)

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Supplementary Information

Additional file 1:.

Demographics and clinical characteristics of study population

Additional file 2:.

Microbiological description of the NON-Ab-PJI group

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da Silva, R.B., Araujo, R.O. & Salles, M.J. Non-elective and revision arthroplasty are independently associated with hip and knee prosthetic joint infection caused by Acinetobacter baumannii: a Brazilian single center observational cohort study of 98 patients. BMC Musculoskelet Disord 22, 511 (2021). https://doi.org/10.1186/s12891-021-04393-4

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