Comparison of Five-Day vs. Fourteen-Day Incubation of Cultures for Diagnosis of Periprosthetic Joint Infection in Hip Arthroplasty
by
, , , ,
Catalina Baez
1,*
,
Robert MacDonell
1,
Abtahi Tishad
2,
Hernan A. Prieto
1,
Emilie N. Miley
1,
Justin T. Deen
3,
Chancellor F. Gray
3,
Hari K. Parvataneni
3 and
Luis Pulido
3,* 1
Department of Orthopaedic Surgery and Sports Medicine, University of Florida, Gainesville, FL 32607, USA
2
College of Medicine, University of Florida, Gainesville, FL 32607, USA
3
Florida Orthopaedic Institute, Gainesville, FL 32607, USA
*
Authors to whom correspondence should be addressed.
J. Clin. Med. 2024, 13(15), 4467; https://doi.org/10.3390/jcm13154467
Submission received: 23 June 2024
/
Revised: 15 July 2024
/
Accepted: 17 July 2024
/
Published: 30 July 2024
(This article belongs to the Special Issue New Advances in Hip and Knee Reconstructive Surgery)
Abstract
:Background: Periprosthetic joint infections (PJI) are among the most morbid complications in total hip arthroplasty (THA). The ideal incubation time, however, for intraoperative cultures for PJI diagnosis remains unclear. As such, the aim of this study was to determine if any differences existed in culture-positive rates and organism detection between five-day and fourteen-day cultures. Methods: This retrospective cohort study consisted of THA cases diagnosed with PJI performed between May 2014 and May 2020 at a single tertiary-care institution. Analyses compared five-day and fourteen-day cultures and carried out a pre-specified subgroup analysis by organism and PJI type. Results: A total of 147 surgeries were performed in 101 patients (57.1% females), of which 65% (n = 98) obtained five-day cultures and 34% (n = 49) obtained fourteen-day cultures. The positive culture rate was 67.3% (n = 99) with Staphylococcus aureus being the most common pathogen identified (n = 41 specimens, 41.4%). The positive culture rate was not significantly different between groups (66.3% five-day, 69.4% fourteen-day, p = 0.852). Fourteen-day cultures had a significantly longer time-to-positive culture (5.0 days) than five-day cultures (3.0 days, p < 0.001), a higher rate of fungi (5.6% vs. 0%), and a lower rate of Gram-negatives (4.5% vs. 18.7%, p = 0.016). Conclusions: Fourteen-day cultures did not increase the positivity rate, had higher rates of slow-growth pathogens, and had a longer time-to-positivization than five-day cultures. Prolonged culture holds may provide more thorough organism detection for PJI without increasing the diagnostic culture yield.
1. Introduction
Prosthetic joint infections (PJI) have a seemingly sparse incidence of 0.76% to 1.24% [1]. However, they are associated with significant morbidity, causing severe psychological [2] and economic [3] burden on the patient, including mortality, with death rates increasing progressively following revision arthroplasty from 5.5 to 8% (1-year postoperative), 11 to 25% (2-years postoperative), and 40 to 45% (5-years postoperative) [4,5,6,7]. In addition, there has been a 2.6-fold increase in annual procedures performed for PJI treatment between 2006 and 2013 [8]. The yearly cost of these procedures exceeded USD 500 million in 2017 and is expected to increase to USD 753.4 million by 2030 [9] as the annual volume of total hip arthroplasty (THA) surgery will increase by 174% by 2030 [1]. This historical increase in the incidence of PJI cases highlights the need for clinicians and researchers to determine the best approach to diagnose PJI.
Released in 2018, the revised Musculoskeletal Infection Society (MSIS) criteria uses a scoring system based on a combination of culture, laboratory, and clinical presentation findings to yield a diagnosis with 99.7% sensitivity and 99.5% specificity [10]. A major criterion for diagnosis is the isolation of a single organism in two separate cultures of periprosthetic tissue or synovial fluid [10]. However, a lack of literature exists to determine the ideal culture time for periprosthetic tissue samples as it appears highly organism-dependent [11,12,13,14,15] with wide variation in incubation times for anaerobic and aerobic samples [16]. A 2018 study demonstrated that while most infected samples yielded positive culture results within five days, some samples (i.e., Cutibacterium acnes (C. acnes)) needed ten or more days to yield positive culture results [11]. Previous PJI diagnosis and management guidelines have failed to address recommendations on the ideal culture incubation duration [10,17,18], and historical trends have proposed culture incubation durations varying from four to fourteen days [12,17].
Considering these inconsistencies in the literature, the aim of this study was to determine if there was a difference in positivity rates, organism growth, time of growth, treatment, and disease-free survival between five-day and fourteen-day cultures in THA PJI. Additionally, we sought to determine the organism profile for PJI in our tertiary-care institution and whether there is an association between preoperative Synovasure® (Zimmer Biomet, Warsaw, IN, USA) synovial fluid cultures and intraoperative culture organism characterization performed at our hospital laboratory.
2. Materials and Methods
After obtaining Institutional Review Board approval, a retrospective cohort study was performed on THA patients diagnosed with PJI from May 2014 through May 2020. Our hospital laboratory transitioned culture hold times in May 2018. Before this time, all cultures were held for five days. Following this transition, cultures were held for fourteen days. All findings from this study are reported following the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [19].
2.1. Participants
The inclusion criteria were THA cases with a diagnosis and treatment for PJI that underwent revision surgery and intraoperative cultures were obtained (CPT codes: 27134, 27137, 27138, 27091, 20680, 11981, 20702, 10061). We included only patients with a minimum one-year follow-up visit. The diagnosis of PJI was based on the 2018 revised MSIS criteria [10]. We excluded all cases where PJI diagnostic criteria were not met, subjects for which intraoperative cultures were not obtained, and patients with less than one-year follow-up.
2.2. Variables and Outcome Measures
Demographic data, including patient medical history (i.e., age, body mass index (BMI), sex), comorbidities (i.e., smoking status, diabetes mellitus (DM)), and PJI data were collected for this study via chart review of the electronic medical record. In addition, perioperative, operative, and postoperative data, surgical and antibiotic treatment, and complications reported during the first year following surgery were collected. Given that the culture hold time was the same for all specimens obtained during each surgery, we compared outcomes across five-day and fourteen-day culture holds by grouping all intraoperative culture specimens into one surgical culture sample (i.e., if one or more of the specimens obtained intraoperatively were positive, this surgical case was determined to be a culture-positive case) for statistical analysis. All organism-specific data were compared using individual culture specimen data for those that reported microbial growth. Thus, the number of intraoperative specimens sent in for culture, the number of specimens that were positive for microbial growth, the time to positive culture, organisms reported, antibiotic selection, definitive surgical intervention (i.e., debridement, antibiotics and implant retention (DAIR), one-stage revision, two-stage revision, resection arthroplasty, and amputation), surgical treatment failure, and disease-free survival were compared using the grouped surgical culture sample data. We defined surgical treatment failure according to the MSIS 2018 consensus [20], where Tiers 3 and 4 represent surgical treatment failure. Disease-free survival was defined as the total follow-up time without further PJI management.
The time to positive culture by organism, type of PJI (i.e., early postoperative, acute hematogenous, and chronic), surgical treatment failure, and complications during the first year after surgery (i.e., readmissions in the first 30 days postoperative and death in the first 365 days postoperative) were obtained to define the PJI organism profile for this institution. Finally, Synovasure® culture reports were collected to compare with intraoperative culture organisms.
2.3. Statistical Analysis
Statistical analyses were performed using the statistical software IBM SPSS Version 28. Categorical measures were summarized as counts (n) and percentages (%), and continuous measures were summarized as means and standard deviations (SD). Categorical variables were analyzed for between-group comparisons with chi-square and Fisher’s exact tests. Given the non-normal characteristics of the data, the Kruskal–Wallis test was used to compare continuous data. Survival analyses were performed using Kaplan–Meier curves and the log-rank test for between-group comparisons. Prespecified subgroup analyses were completed for low-virulence organisms (i.e., C. acnes, Cutibacterium albicans (C. albicans), mycobacteria, and anaerobes) and different organism types (i.e., Gram-positive, Gram-negative, anaerobes, fungi). Disease-free survival was defined as the total follow-up time without further PJI management, and case censoring was defined as surgical treatment failure according to the MSIS 2018 consensus [10]. Statistical significance was predefined at a p < 0.05.
3. Results
A total of 147 surgeries were identified for 101 patients with a PJI diagnosis from May 2014 to May 2020. Of these, 66.7% (n = 98) of the surgical culture samples were held for five days, and 33.3% (n = 49) were held for fourteen days. In total, 57.1% (n = 84) were male, and 63% (n = 42.9) were female, with a mean age of 62.0 (±12.7) years and a mean BMI of 30.8 (±9.0). A total of 19% (n = 28) of the patients in the sample reported being active smokers at the time of PJI diagnosis, and 32% (n = 47) had a diagnosis of diabetes mellitus (DM). The McPherson host grade [21] rates were 12.2% (n = 18) grade A, 46.3% (n = 68) grade B, and 41.5% (n = 61) grade C. Additionally, 71.4% (n = 105) of cases were classified as chronic PJI, 15.6% (n = 23) as acute hematogenous, and 12.9% (n = 19) as early postoperative. No significant differences were identified for patient demographics between the five-day and fourteen-day groups (Table 1).
3.1. Comparison of Five-Day and Fourteen-Day Cultures
The culture-positive rate for the full cohort was 67.3% (n = 99), with no significant differences between five-day and fourteen-day cultures (p = 0.852, Table 2). The mean number of individual specimens obtained during each surgery was 8.0 (±4.2), of which a mean of 2.5 (±1.4) specimens grew detectable organisms. There was no significant differences between five-day and fourteen-day cultures for the total number of specimens sent for culture (p = 0.079) or the number of positive specimens (p = 0.527, Table 2).
The median time to positive culture was 4.0 days (range = 0–23 days). The time to positive culture was significantly longer for fourteen-day cultures with a median time of 5.0 days (range = 0–23 days), whereas the five-day cultures had a median of 3.0 days (range = 0–7 days, p < 0.001; Table 2). No significant differences were identified for the mono- and polymicrobial infections between five-day and fourteen-day cultures (p = 0.135; Table 2). Of the sample, Staphylococcus aureus (S. aureus) was the most detected organism, found in 34.4% (n = 41) of all positive specimens. Of these, methicillin-resistant S. aureus (MRSA) was present in 48.8% (n = 20) of the specimens, and methicillin-sensitive S. aureus (MSSA) was present in the remaining 51.2% (n = 21). No significant difference was identified between MRSA and MSSA rates between the five-day and fourteen-day cultures (p = 0.541; Table 2). However, the rates pertaining to the different types of organisms detected were significantly different between groups (p = 0.016; Table 2). Fungi were only detected in fourteen-day holds (4.5%, n = 2). Five-day holds had higher rates of Gram-negatives (18.7%, n = 14) and anaerobes (1.3%, n = 1). Gram-positives comprised the most common type of organism and were detected in both groups (Table 2).
The use of postoperative broad-spectrum antibiotics and culture-specific monotherapy was similar between the five-day and fourteen-day cultures (p = 0.996); additionally, definitive surgical management was also similar across groups (p = 0.196, Table 2). The surgical treatment failure rate was higher for the five-day cultures than for the fourteen-day cultures (74.5%, n = 73 vs. 59.2%, n = 29, respectively, p = 0.087), though not significantly different. Of these, 32.4% (n = 33) were reported in culture-negative cases and 67.6% (n = 69) in culture-positive cases. Kaplan–Meier survival curves reported a median disease-free survival of 226.0 weeks (95% CI: 106.9–345.1, Figure 1). The curve comparison using the log-rank test showed a significant difference between the survival curves for five-day and fourteen-day cultures (p = 0.043). Also, the median disease-free survival in the five-day cultures was 226.0 weeks (95% CI: 79.2–372.8) and it was 104.0 weeks in the fourteen-day cultures (95% CI: 65.2–142.8).
3.2. Institutional Organism Profile
The time to positive culture by organism was significantly different, as Trichosporon sp. had the longest median time to positive (i.e., 23 days) and Finegoldia magna had the shortest (i.e., 0 days, p = 0.011). Subgroup analysis for low-virulence organisms demonstrated no significant difference between C. acnes, C. albicans, mycobacteria, and anaerobes (p = 0.407; Table 3). The time to positive culture by organism type was not statistically significant (p = 0.063; Table 3).
The rates of mono- and polymicrobial infections across PJI types were not significantly different (p = 0.492; Table 4). Additionally, the types of organism across types of PJI were not significantly different (p = 0.312; Table 4). However, surgical treatment failure was reported in 69.4% (n = 102) of cases. The comparison by PJI type was not statistically significant (p = 0.107), with chronic PJI in 76.5% (n = 78) of cases, acute hematogenous in 13.7% (n = 14) of cases, and early postoperative in 9.8% (n = 10; Table 5) of cases. When analyzed by the type of organism with mono- and polymicrobial infections, no significant differences were identified across the rates of surgical treatment failure (p = 0.394 and p = 1.000, respectively; Table 5).
Postoperative complication rates were compared across types of PJI, organisms, and colonization. Deaths during the first 365 days after surgery were reported in 2.0% of cases (n = 3). Comparison by PJI type was not statistically significant (p = 1.000), with chronic PJI identified in 66.7% (n = 2) of cases, followed by acute hematogenous in 33.3% (n = 1), and no reported deaths for early postoperative PJIs (Table 5). Similarly, when analyzed by the type of organism and mono- and polymicrobial infections, no significant differences were identified across mortality rates (p = 0.080 and p = 0.315, respectively, Table 5). Readmissions during the first 30 days after surgery were reported in 22.4% (n = 33) of cases. The comparison by organism type was statistically significant (p = 0.050), with Gram-positive organisms identified in 81.0% (n = 17) of cases, followed by Gram-negative organisms (4.8%, n = 1), fungi (4.8%, n = 1), and anaerobes (4.8%, n = 1). However, when analyzed by type of infection, organism, and mono- and polymicrobial infections, no significant differences were identified across readmission rates (p = 0.360, p = 0.114, and p = 1.000, respectively; Table 5).
3.3. Association of Synovial and Intraoperative Cultures
Preoperatively, 29.9% (n = 44) of cases had a Synovasure® test administered; of these, 70.5% (n = 31) reported negative organism detection, and the remaining 29.5% (n = 13) reported positive organism detection. However, no significant association existed between the organisms reported in Synovasure® testing and the intraoperative cultures (p = 0.234). Only six Synovasure® cases accurately reported the same organism found in intraoperative cultures. The congruently reported microorganisms in both tests were S. agalactie, MRSA, MSSA, coagulase-negative S. aureus, S. epidermidis, and C. acnes. The organisms that were reported in the intraoperative cultures but not in the preoperative Synovasure® testing were E. faecium, Bacillus sp., Corynebacterium sp., E. coli, E. faecalis, K. pneumoniae, S. viridans, and C. albicans.
4. Discussion
Our results demonstrated that fourteen-day cultures had a median growth time that was significantly longer and included higher rates of fungi detection than those held for five days. Previous literature has reported similar findings where other slow-growth organisms, like C. acnes, were detected during the second week of culture [12,22,23]. However, our findings show a median time to positive culture for C. acnes of 8.50 days (Table 3), further supporting the idea that shorter culture times potentially miss the diagnosis of slow-growing organisms.
Disease-free survival following surgical intervention for PJI was significantly longer for patients in the five-day culture group than in the fourteen-day culture group. However, the interpretation of these findings must consider lead-time bias, as the institutional shift from shorter to longer culture hold times was time-dependent. Patients in the fourteen-day cohort have yet to be followed long enough to deem this difference clinically significant. Our results failed to demonstrate a significant difference between culture hold times for the number of tissue samples sent for culture, the number of positive tissue samples, the rates of MRSA and MSSA, antibiotic coverage, and definitive surgical management of the PJI. Our findings reiterate those of Klement et al., who also failed to find a significant association between an improved surgical success of PJI treatment and more prolonged culture holds [15].
We found the culture positive rate to be similar across hold times, thus not increasing culture yield. This reiterates previous studies looking at similar comparisons [14,15]. However, it is important to note that other researchers have identified up to a 30% increase in positivity rate for longer culture times [12]. Previous literature, however, has reported concerns with the utility of longer culture times and the risk of an increased detection of contaminating organisms [12,14,15]. Although our results support previous findings on similar rates of polymicrobial infections across culture hold times [15], some organisms commonly categorized as contaminants [12,24] were identified in these polymicrobial cultures, primarily in those in the fourteen-day culture group. As such, there continues to be inconsistency regarding prolonged culture, which holds a risk of higher contamination rates as these organisms also have the potential for infection [12,24].
The most common organism detected in this sample was S. aureus, followed by coagulase-negative Staphylococcus species, which is consistent with epidemiological reports of PJI microbiology [13,25,26]. The time to positive culture was significantly different when compared by organism type; the largest difference was between fungi and Gram-negative organisms’ growth time (Table 3). However, this finding was not the case for low virulence organisms; the median growth time identified for this subgroup was 6.14 days. Both of these findings underscore the potential effect of prolonged culture holds. Significant differences in growth time between commonly slow-growing organisms (e.g., fungi) and faster-growing organisms (e.g., Gram-negatives), and the similarity among organisms considered “low virulence” point to more extended culture holds, allowing for sufficient time to detect these organisms in a sample [12,27].
Our cohort’s surgical treatment failure rate was higher than other rates reported in the literature [28,29,30]. However, there is inconsistency regarding the definition of treatment failure present in these studies. Most treatment failure cases were in the five-day culture group, with one-third of failures reported in culture-negative cases. These findings underscore the significance of determining the best available culture hold time. In our study, subgroup analyses did not reveal significant differences across PJI types, organism, and colonization types, which is also supported by previous research that has identified no association between the organism and colonization type and failure rates [31].
Finally, no significant association was identified between the organisms reported from intraoperative cultures and Synovasure® cultures, with only six cases accurately reporting the same organism in both cultures. However, Synovasure® testing reported negative culture results in multiple cases where intraoperative cultures reported organisms commonly qualified as contaminants. This descriptive trend in the data highlights the potential for the culture overgrowth of environmental contaminants, a common pitfall in extended bacterial culture sampling [12,24]. However, clinicians must be mindful that common culture contaminants can also overgrow and cause PJI, regardless of their categorization [12]. Thus, the correlation between intraoperative culture, Synovasure® results, and clinical and laboratory findings is imperative when determining diagnosis, management, and antibiotic coverage [10]. Our findings are echoed by a previous systematic review that identified variable concordance between Synovasure® and intraoperative cultures [32]. Previous research in this institution has supported the use of the Synovasure® test’s alpha-defensin levels to have high sensitivity in PJI diagnosis and specificity following two-stage reimplantation [33,34]. However, further research is necessary to evaluate the role of Synovasure® cultures compared to intraoperative cultures. It remains unclear if there is any association between these results and the length of intraoperative culture hold, as this was not the goal of this study.
The results must be interpreted considering the limitations of this study. First, the retrospective nature of this study introduces an opportunity for selection and lead-time bias. This limitation becomes more important for disease-free survival comparisons, with five-day cultures being the standard of care during the first four years of data collection and fourteen-day cultures for the last two years of data collection. Patients who were diagnosed using five-day cultures were inherently followed for a longer period than the fourteen-day culture patients. Second, there was a relatively small sample size of 147 surgical culture samples for analysis. However, given that this study aimed to analyze outcomes from an uncommon, but impactful, complication of total joint arthroplasty, this sample size and methodology are justifiable and comparable to similar studies. Third, there was an unbalanced sample size between five-day and fourteen-day cultures. Although this distribution of samples was expected due to the period analyzed, this imbalance may impact the study’s statistical power. However, in findings where statistical significance was identified to favor the fourteen-day cultures, this 2:1 sample distribution underscores the meaningfulness of these differences. Fourth, as this study was performed at a single institution, this may limit the generalizability of the results. However, surgeries were performed by eight different fellowship-trained arthroplasty surgeons, introducing variability into the dataset and expanding the applicability of the results. Future research should focus on longer culture holds and sensitivity and specificity regarding contaminant organism detection. Similarly, investigation into the cost-effectiveness of longer culture holds and the potential impact on accurate organism detection and PJI management is needed, as it becomes increasingly clear that there continues to be potential benefits in longer culture holds.
5. Conclusions
This retrospective cohort study revealed that fourteen-day cultures did not increase the positivity rate, rate of polymicrobial infections, or number of positive specimens reported, and it also identified a similar disease-free survival to five-day cultures. Fourteen-day culture holds demonstrated higher fungi growth rates and a longer time-to-positivization than five-day cultures. More prolonged culture holds may provide a more thorough organism detection for PJI; however, the risk of contaminant over-detection remains. In light of these findings, arthroplasty surgeons should consider increasing intraoperative culture hold times to fourteen days due to the potential for the increased detection of low-virulence organisms known for introducing complexity to managing PJI cases.
Author Contributions
Conceptualization, C.B., L.P. and R.M.; methodology C.B., L.P. and R.M.; software, C.B.; validation, C.B., A.T. and R.M.; formal analysis, C.B.; investigation, C.B., L.P. and R.M.; data curation, C.B., A.T. and R.M.; writing—original draft preparation, C.B., A.T. and L.P.; writing—review and editing, H.A.P., E.N.M., J.T.D., C.F.G., H.K.P. and L.P.; supervision, L.P.; project administration, E.N.M. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of University of Florida IRB202001322 approved on 15 June 2020.
Informed Consent Statement
Patient consent was waived due to this study being a retrospective chart review.
Data Availability Statement
The dataset analyzed during the study are not publicly available per study protocol. De-identified data may be available from the corresponding author with permission from the University of Florida upon reasonable request.
Conflicts of Interest
The authors declare no conflicts of interest.
References
- Springer, B.D.; Cahue, S.; Etkin, C.D.; Lewallen, D.G.; McGrory, B.J. Infection burden in total hip and knee arthroplasties: An international registry-based perspective. Arthroplast. Today 2017, 3, 137–140. [Google Scholar] [CrossRef]
- Andersson, A.E.; Bergh, I.; Karlsson, J.; Nilsson, K. Patients’ experiences of acquiring a deep surgical site infection: An interview study. Am. J. Infect. Control 2010, 38, 711–717. [Google Scholar] [CrossRef]
- Kurtz, S.M.; Lau, E.; Watson, H.; Schmier, J.K.; Parvizi, J. Economic burden of periprosthetic joint infection in the United States. J. Arthroplast. 2012, 27, 61–65.e1. [Google Scholar] [CrossRef] [PubMed]
- Zmistowski, B.; Karam, J.A.; Durinka, J.B.; Casper, D.S.; Parvizi, J. Periprosthetic joint infection increases the risk of one-year mortality. J. Bone Jt. Surg. Am. 2013, 95, 2177–2184. [Google Scholar] [CrossRef] [PubMed]
- Petis, S.M.; Abdel, M.P.; Perry, K.I.; Mabry, T.M.; Hanssen, A.D.; Berry, D.J. Long-Term Results of a 2-Stage Exchange Protocol for Periprosthetic Joint Infection Following Total Hip Arthroplasty in 164 Hips. J. Bone Jt. Surg. Am. 2019, 101, 74–84. [Google Scholar] [CrossRef]
- Kildow, B.J.; Springer, B.D.; Brown, T.S.; Lyden, E.; Fehring, T.K.; Garvin, K.L. Long Term Results of Two-Stage Revision for Chronic Periprosthetic Hip Infection: A Multicenter Study. J. Clin. Med. 2022, 11, 1657. [Google Scholar] [CrossRef] [PubMed]
- Fischbacher, A.; Borens, O. Prosthetic-joint Infections: Mortality Over the Last 10 Years. J. Bone Jt. Infect. 2019, 4, 198–202. [Google Scholar] [CrossRef] [PubMed]
- Lenguerrand, E.; Whitehouse, M.R.; Beswick, A.D.; Jones, S.A.; Porter, M.L.; Blom, A.W. Revision for prosthetic joint infection following hip arthroplasty: Evidence from the National Joint Registry. Bone Jt. Res. 2017, 6, 391–398. [Google Scholar] [CrossRef]
- Premkumar, A.; Kolin, D.A.; Farley, K.X.; Wilson, J.M.; McLawhorn, A.S.; Cross, M.B.; Sculco, P.K. Projected economic burden of periprosthetic joint infection of the hip and knee in the united states. J. Arthroplast. 2021, 36, 1484–1489.e3. [Google Scholar] [CrossRef]
- Parvizi, J.; Tan, T.L.; Goswami, K.; Higuera, C.; Della Valle, C.; Chen, A.F.; Shohat, N. The 2018 Definition of Periprosthetic Hip and Knee Infection: An Evidence-Based and Validated Criteria. J. Arthroplast. 2018, 33, 1309–1314.e2. [Google Scholar] [CrossRef]
- Kheir, M.M.; Tan, T.L.; Ackerman, C.T.; Modi, R.; Foltz, C.; Parvizi, J. Culturing periprosthetic joint infection: Number of samples, growth duration, and organisms. J. Arthroplast. 2018, 33, 3531–3536.e1. [Google Scholar] [CrossRef] [PubMed]
- Schäfer, P.; Fink, B.; Sandow, D.; Margull, A.; Berger, I.; Frommelt, L. Prolonged bacterial culture to identify late periprosthetic joint infection: A promising strategy. Clin. Infect. Dis. 2008, 47, 1403–1409. [Google Scholar] [CrossRef]
- Talsma, D.T.; Ploegmakers, J.J.W.; Jutte, P.C.; Kampinga, G.; Wouthuyzen-Bakker, M. Time to positivity of acute and chronic periprosthetic joint infection cultures. Diagn. Microbiol. Infect. Dis. 2021, 99, 115178. [Google Scholar] [CrossRef]
- Esteban, J.; Alvarez-Alvarez, B.; Blanco, A.; Fernández-Roblas, R.; Gadea, I.; Garcia-Cañete, J.; Sandoval, E.; Valdazo, M. Prolonged incubation time does not increase sensitivity for the diagnosis of implant-related infection using samples prepared by sonication of the implants. Bone Jt. J. 2013, 95-B, 1001–1006. [Google Scholar] [CrossRef]
- Klement, M.R.; Cunningham, D.J.; Wooster, B.M.; Wellman, S.S.; Bolognesi, M.P.; Green, C.L.; Garrigues, G.E. Comparing standard versus extended culture duration in acute hip and knee periprosthetic joint infection. J. Am. Acad. Orthop. Surg. 2019, 27, e437–e443. [Google Scholar] [CrossRef] [PubMed]
- Yusuf, E.; Roschka, C.; Esteban, J.; Raglio, A.; Tisler, A.; Willems, P.; Kramer, T.S. The State of Microbiology Diagnostic of Prosthetic Joint Infection in Europe: An In-Depth Survey Among Clinical Microbiologists. Front. Microbiol. 2022, 13, 906989. [Google Scholar] [CrossRef]
- Osmon, D.R.; Berbari, E.F.; Berendt, A.R.; Lew, D.; Zimmerli, W.; Steckelberg, J.M.; Rao, N.; Hanssen, A.; Wilson, W.R. Diagnosis and Management of Prosthetic Joint Infection: Clinical Practice Guidelines by the Infectious Diseases Society of America. Clin. Infect. Dis. 2013, 56, e1–e25. [Google Scholar] [CrossRef]
- American Academy of Orthopaedic Surgeons Evidence-Based Clinical Practice Guideline for Diagnosis and Prevention of Periprosthetic Joint Infections, AAOS. 2019. Available online: https://www.aaos.org/pjicpg (accessed on 14 February 2024).
- von Elm, E.; Altman, D.G.; Egger, M.; Pocock, S.J.; Gøtzsche, P.C.; Vandenbroucke, J.P. STROBE Initiative the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. Ann. Intern. Med. 2007, 147, 573–577. [Google Scholar] [CrossRef]
- Fillingham, Y.A.; Della Valle, C.J.; Suleiman, L.I.; Springer, B.D.; Gehrke, T.; Bini, S.A.; Segreti, J.; Chen, A.F.; Goswami, K.; Tan, T.L.; et al. Definition of successful infection management and guidelines for reporting of outcomes after surgical treatment of periprosthetic joint infection: From the workgroup of the musculoskeletal infection society (MSIS). J. Bone Jt. Surg. Am. 2019, 101, e69. [Google Scholar] [CrossRef]
- Coughlan, A.; Taylor, F. Classifications in brief: The McPherson classification of periprosthetic infection. Clin. Orthop. Relat. Res. 2020, 478, 903–908. [Google Scholar] [CrossRef]
- Butler-Wu, S.M.; Burns, E.M.; Pottinger, P.S.; Magaret, A.S.; Rakeman, J.L.; Matsen, F.A.; Cookson, B.T. Optimization of periprosthetic culture for diagnosis of Propionibacterium acnes prosthetic joint infection. J. Clin. Microbiol. 2011, 49, 2490–2495. [Google Scholar] [CrossRef] [PubMed]
- Renz, N.; Mudrovcic, S.; Perka, C.; Trampuz, A. Orthopedic implant-associated infections caused by Cutibacterium spp.—A remaining diagnostic challenge. PLoS ONE 2018, 13, e0202639. [Google Scholar] [CrossRef] [PubMed]
- Hall, K.K.; Lyman, J.A. Updated review of blood culture contamination. Clin. Microbiol. Rev. 2006, 19, 788–802. [Google Scholar] [CrossRef]
- Esposito, S.; Leone, S. Prosthetic joint infections: Microbiology, diagnosis, management and prevention. Int. J. Antimicrob. Agents 2008, 32, 287–293. [Google Scholar] [CrossRef] [PubMed]
- Del Pozo, J.L.; Patel, R. Clinical practice. Infection associated with prosthetic joints. N. Engl. J. Med. 2009, 361, 787–794. [Google Scholar] [CrossRef]
- Gupta, V.; Kaur, M.; Bora, P.; Kumari, P.; Datta, P.; Gupta, R.; Chander, J. A prospective study to assess the optimal incubation times for culture and aerobic bacterial profile in prosthetic joint infections. J. Lab. Physicians 2021, 13, 224–230. [Google Scholar] [CrossRef] [PubMed]
- View of Risk of Treatment Failure for Prosthetic Joint Infections: Retrospective Chart Review in an Outpatient Parenteral Antimicrobial Therapy Program|Canadian J. Hosp. Pharm. 2023, 76, 1. Available online: https://www.cjhp-online.ca/index.php/cjhp/article/view/3264/4835 (accessed on 31 October 2023).
- Kandel, C.E.; Jenkinson, R.; Daneman, N.; Backstein, D.; Hansen, B.E.; Muller, M.P.; Katz, K.C.; Widdifield, J.; Bogoch, E.; Ward, S.; et al. 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, ofz452. [Google Scholar] [CrossRef]
- Espíndola, R.; Vella, V.; Benito, N.; Mur, I.; Tedeschi, S.; Zamparini, E.; Hendriks, J.G.E.; Sorlí, L.; Murillo, O.; Soldevila, L.; et al. ARTHR-IS Group Rates and Predictors of Treatment Failure in Staphylococcus aureus Prosthetic Joint Infections According to Different Management Strategies: A Multinational Cohort Study-The ARTHR-IS Study Group. Infect. Dis. Ther. 2022, 11, 2177–2203. [Google Scholar] [CrossRef]
- Flaten, D.; Berrigan, L.; Spirkina, A.; Gin, A. Risk of treatment failure for prosthetic joint infections: Retrospective chart review in an outpatient parenteral antimicrobial therapy program. Can. J. Hosp. Pharm. 2023, 76, 14–22. [Google Scholar] [CrossRef]
- van Schaik, T.J.A.; de Jong, L.D.; van Meer, M.P.A.; Goosen, J.H.M.; Somford, M.P. The concordance between preoperative synovial fluid culture and intraoperative tissue cultures in periprosthetic joint infection: A systematic review. J. Bone Jt. Infect. 2022, 7, 259–267. [Google Scholar] [CrossRef]
- Stone, W.Z.; Gray, C.F.; Parvataneni, H.K.; Al-Rashid, M.; Vlasak, R.G.; Horodyski, M.; Prieto, H.A. Clinical Evaluation of Synovial Alpha Defensin and Synovial C-Reactive Protein in the Diagnosis of Periprosthetic Joint Infection. J. Bone Jt. Surg. Am. 2018, 100, 1184–1190. [Google Scholar] [CrossRef]
- Stone, W.Z.; Gray, C.F.; Parvataneni, H.K.; Prieto, H.A. Clinical evaluation of alpha defensin test following staged treatment of prosthetic joint infections. J. Arthroplasty 2019, 34, 1446–1451. [Google Scholar] [CrossRef]
Figure 1.
Kaplan–Meier curves for disease-free survival for five-day and fourteen-day culture cases.
Figure 1.
Kaplan–Meier curves for disease-free survival for five-day and fourteen-day culture cases.
Table 1.
Patient demographics.
| Total N = 147 | 5-Day Cultures N = 98 | 14-Day Cultures N = 49 | p-Value | |
|---|---|---|---|---|
| Age, mean (SD) | 62.0 (12.7) | 61.5 (12.1) | 61.4 (12.7) | 0.976 |
| BMI, mean (SD) | 30.8 (9.1) | 30.2 (8.8) | 31.2 (7.6) | 0.612 |
| Sex, n (%) | 0.216 | |||
| Female | 63 (42.9) | 38 (38.8) | 25 (51.0) | |
| Male | 84 (57.1) | 60 (61.2) | 24 (49.0) | |
| McPherson Host Grade, n (%) | 0.249 | |||
| A | 18 (12.2) | 15 (15.3) | 3 (6.1) | |
| B | 68 (46.3) | 45 (45.9) | 23 (46.9) | |
| C | 61 (41.5) | 38 (38.8) | 23 (46.9) | |
| Active Smoking, n (%) | 28 (19.0) | 20 (20.4) | 8 (16.3) | 0.710 |
| DM, n (%) | 47 (32.0) | 33 (33.7) | 14 (28.6) | 0.662 |
| Laterality, n (%) | 0.600 | |||
| Left | 72 (49.0) | 46 (46.9) | 26 (53.1) | |
| Right | 75 (51.0) | 52 (53.1) | 23 (46.9) | |
| Periprosthetic Joint Infection Type, n (%) | 0.976 | |||
| Early Postoperative | 19 (12.9) | 13 (13.3) | 6 (12.2) | |
| Acute Hematogenous | 23 (15.6) | 15 (15.3) | 8 (16.3) | |
| Chronic | 105 (71.4) | 70 (71.4) | 35 (71.4) |
Abbreviations—BMI: body mass index; DM: diabetes mellitus type II.
Table 2.
Comparison between 5-day and 14-day cultures.
| Total N = 147 | 5-Day Cultures N = 98 | 14-Day Cultures N = 49 | p-Value | |
|---|---|---|---|---|
| Culture Positive Rate, n (%) | 99 (67.3) | 65 (66.3) | 34 (69.4) | 0.852 |
| Intraoperative Specimens, Mean (SD) | 8.0 (4.2) | 8.3 (3.9) | 7.6 (4.9) | 0.079 |
| Positive Specimens, Mean (SD) | 2.5 (1.4) | 2.6 (1.5) | 2.4 (1.4) | 0.527 |
| Time to Positive Culture, Median (Range) | 4.0 (0–23) | 3.0 (0–7) | 5.0 (0–23) | <0.001 |
| Colonization, n (%) | 0.135 | |||
| Monomicrobial | 82 (82.2) | 57 (87.7) | 25 (73.5) | |
| Polymicrobial | 17 (17.2) | 8 (12.3) | 9 (26.5) | |
| S. aureus sensitivities, n (%) | 0.541 | |||
| MRSA | 20 (48.8) | 16 (53.3) | 4 (36.4) | |
| MSSA | 21 (51.2) | 14 (46.7) | 7 (63.6) | |
| Organism Type, n (%) | 0.016 | |||
| Gram-Positive | 100 (84.0) | 60 (80.0) | 40 (90.9) | |
| Gram-Negative | 16 (13.4) | 14 (18.7) | 2 (4.5) | |
| Anaerobe | 1 (0.8) | 1 (1.3) | 0 (0.0) | |
| Fungi | 2 (1.7) | 0 (0.0) | 2 (4.5) | |
| Definitive Surgery, n (%) | 0.196 | |||
| DAIR | 24 (16.3) | 16 (16.3) | 8 (16.3) | |
| 1-Stage | 33 (22.4) | 18 (18.4) | 15 (30.6) | |
| 2-Stage | 73 (49.7) | 49 (50.0) | 24 (49.0) | |
| Resection Arthroplasty | 16 (10.9) | 14 (14.3) | 2 (4.1) | |
| Amputation | 1 (0.7) | 1 (1.0) | 0 (0.0) | |
| Antibiotic Spectrum, n (%) | 0.724 | |||
| Narrow | 8 (6.7) | 6 (7.4) | 2 (5.3) | |
| Broad | 111 (93.3) | 75 (92.6) | 36 (94.7) | |
| Surgical Treatment Failure, n (%) | 102 (69.4) | 73 (71.6) | 29 (28.4) | 0.087 |
Abbreviations—MRSA: methicillin-resistant Staphylococcus aureus; MSSA: methicillin-sensitive Staphylococcus aureus; DAIR: debridement, antibiotics, and implant retention. Bolded: statistically significant.
Table 3.
Comparison between 5-day and 14-day cultures.
| Individual Organism N (%) | Time to Positive Culture Median Days (Range) | p-Value | |
|---|---|---|---|
| Organism Type (n = 119) | 0.063 | ||
| Gram-Positive | 100 (84.0) | 4.0 (0–11) | |
| Gram-Negative | 16 (13.4) | 3.5 (3–4) | |
| Anaerobes * | 1 (0.8) | 0.00 (0) | |
| Fungi | 2 (1.7) | 14.5 (6–23) | |
| Low Virulence Organisms (n = 8) | 0.407 | ||
| C. acnes | 5 (4.2) | 8.5 (2–11) | |
| C. albicans | 1 (0.8) | 6.0 (6) | |
| Mycobacteria ** | 1 (0.8) | 7.0 (7) | |
| Anaerobes * | 1 (0.8) | 0.0 (0) |
* Only one obligate anaerobe was identified within the sample, Finegoldia magna, and was reported as positive in culture on the same day the sample was sent for culture. ** One type of mycobacteria was identified, Mycobacteria fortuitum, and E. coli was the only Gram-negative organism identified.
Table 4.
Comparisons by PJI type.
| Total n (%) | Early Postoperative n (%) | Acute Hematogenous n (%) | Chronic n (%) | p-Value * | |
|---|---|---|---|---|---|
| Colonization | 0.492 | ||||
| Monomicrobial | 82 (82.8) | 14 (82.4) | 16 (94.1) | 52 (80.0) | |
| Polymicrobial | 17 (17.2) | 3 (17.6) | 1 (5.9) | 13 (20.0) | |
| Organism Type | 0.250 | ||||
| Gram-Positive | 100 (84.0) | 17 (81.0) | 11 (94.4) | 66 (82.5) | |
| Gram-Negative | 16 (13.4) | 2 (9.5) | 1 (5.6) | 13 (16.3) | |
| Anaerobes | 1 (0.8) | 1 (4.8) | 0 (0.0) | 0 (0.0) | |
| Fungi | 2 (1.7) | 1 (4.8) | 0 (0.0) | 1 (1.3) |
Table 5.
Complications and surgical treatment failure comparisons across PJI types.
| 30-Day Readmissions n (%) | p-Value | 365-Day Mortality n (%) | p-Value | Surgical Treatment Failure n (%) | p-Value | |
|---|---|---|---|---|---|---|
| Colonization | 1.000 | 0.315 | 1.000 | |||
| Monomicrobial | 17 (81.0) | 1 (50.0) | 57 (82.6) | |||
| Polymicrobial | 4 (19.0) | 1 (50.0) | 12 (17.4) | |||
| Organism Type | 0.114 | 0.180 | 0.394 | |||
| Gram-Positive | 19 (70.4) | 2 (50.0) | 65 (80.2) | |||
| Gram-Negative | 7 (25.9) | 2 (50.0) | 13 (16.0) | |||
| Anaerobes | 0 (0.0) | 0 (0.0) | 1 (1.2) | |||
| Fungi | 1 (3.7) | 0 (0.0) | 2 (2.5) | |||
| PJI Type | 0.360 | 1.000 | 0.107 | |||
| Early Postoperative | 3 (9.1) | 0 (0.0) | 10 (12.9) | |||
| Acute Hematogenous | 3 (9.1) | 1 (33.3) | 14 (13.7) | |||
| Chronic | 27 (81.8) | 2 (66.7) | 78 (76.5) |
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Baez, C.; MacDonell, R.; Tishad, A.; Prieto, H.A.; Miley, E.N.; Deen, J.T.; Gray, C.F.; Parvataneni, H.K.; Pulido, L. Comparison of Five-Day vs. Fourteen-Day Incubation of Cultures for Diagnosis of Periprosthetic Joint Infection in Hip Arthroplasty. J. Clin. Med. 2024, 13, 4467. https://doi.org/10.3390/jcm13154467
AMA Style
Baez C, MacDonell R, Tishad A, Prieto HA, Miley EN, Deen JT, Gray CF, Parvataneni HK, Pulido L. Comparison of Five-Day vs. Fourteen-Day Incubation of Cultures for Diagnosis of Periprosthetic Joint Infection in Hip Arthroplasty. Journal of Clinical Medicine. 2024; 13(15):4467. https://doi.org/10.3390/jcm13154467
Chicago/Turabian StyleBaez, Catalina, Robert MacDonell, Abtahi Tishad, Hernan A. Prieto, Emilie N. Miley, Justin T. Deen, Chancellor F. Gray, Hari K. Parvataneni, and Luis Pulido. 2024. "Comparison of Five-Day vs. Fourteen-Day Incubation of Cultures for Diagnosis of Periprosthetic Joint Infection in Hip Arthroplasty" Journal of Clinical Medicine 13, no. 15: 4467. https://doi.org/10.3390/jcm13154467
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