Abstract
Background
Osteomyelitis-complicating pressure ulcers are frequent among patients with spinal cord injuries (SCIs), and the optimal management is unknown. In our referral center, the current management is debridement and flap coverage surgeries, followed by a short antibiotic treatment. We aimed to evaluate patients’ outcomes a year after surgery.
Methods
We performed a quasi-experimental retrospective before/after study on SCI patients with presumed osteomyelitis associated with perineal pressure ulcers. We included all patients who underwent surgery with debridement and flap covering, followed by effective antibiotic treatment, between May 1, 2016, and October 30, 2020. The effective antimicrobial treatment duration included the 10 days leading up to January 1, 2018 (before period), and the 5 to 7 days after (after period). We also compared the efficacy of 5–7-day vs 10-day antibiotic treatment and performed uni- and multivariable analyses to identify factors associated with failure.
Results
Overall, 415 patients were included (77.6% male patients; mean age ± SD, 53.0 ± 14.4 years). Multidrug-resistant organisms (MDROs) were involved in 20.7% of cases. Favorable outcomes were recorded in 69.2% of cases: 117/179 (65.3%) in the 10-day treatment group vs 169/287 (71.9%) in the 5–7-day treatment group (P = .153). The only factor associated with failure in the multivariate analysis was a positive culture from suction drainage (odds ratio, 1.622; 95% CI, 1.005–2.617; P = .046). Effective treatment duration >7 days and intraoperative samples negative for MDROs were not associated with better outcomes (P = .153 and P = .241, respectively).
Conclusions
A treatment strategy combining surgical debridement and flap covering, followed by 5 to 7 days of effective antibiotic treatment seems safe.
Keywords: MDRO, antibiotics, osteomyelitis, pressure ulcer, treatment duration
The spinal cord injured (SCI) population is subject to pressure ulcers because of numerous risk factors: neurological disorders, which reduce ability to mobilize, potential undernutrition, confinement to bed, and vascular disorders promoting the lesions. Pressure ulcers often lead to osteomyelitis in the absence of adequate care. Despite the attention given to preventative strategies, in the SCI population, the prevalence of pressure ulcers varies from 10% to 30%, with an annual incidence rate ranging from 20% to 31% [1–3].
In the community-dwelling SCI population, osteomyelitis-complicating pressure ulcers requiring surgical intervention account for 25% of total ulcers observed [1]. It is a major cause of health care center admissions and home care nursing [4]. The occurrence of a pressure ulcer, especially with osteomyelitis, is associated with potential several hospitalizations and with a longer length of stay [1, 5–7]. Therefore, pressure ulcers with osteomyelitis are an important economic burden to the health care system.
A recent review did not find evidence of benefit of antibacterial therapy in osteomyelitis associated with pressure ulcers without concomitant surgical debridement and wound coverage [8]. But management of this setting is still controversial [8, 9].
In our center, patients benefit from a 1-stage surgical management with bone shaving and flap covering osteitis of the pressure ulcer to perform wound closing. Surgery is followed by empiric treatment, then tailored to match the intraoperative cultures for the remaining duration of therapy.
Furthermore, the management of each SCI patient is protocolized in a specific care pathway, comprised of preoperative evaluation, especially of nutritional status, and a strict postoperative rehabilitation program an with off-loading protocol (no support during the first 6 weeks then 1 hour each week until 12 weeks), to limit the failure rate.
Thus, we aimed to evaluate this original strategy and performed a before/after study comparing 5–7 days with 10 days of effective antibiotic treatment. We also identified factors associated with failure.
METHODS
We performed a quasi-experimental retrospective before/after cohort study in a university hospital, which is a referral center for bone and joint infections.
We included all adult patients with presumed osteomyelitis complicating perineal (ischial, sacrum, and trochanter) pressure ulcers who underwent surgery and had significant microbiological identification on intraoperative samples between May 1, 2016, and October 30, 2020. We considered that exposed bone with positive intraoperative samples meant osteomyelitis, as histology analysis is not routinely performed in our center.
We excluded patients with concomitant infections, patients with absence of associated osteomyelitis or positive intraoperative samples, patient who were lost to follow-up, and patients without antibiotic treatment.
The surgery performed was a large debridement and deep bone shaving, then closure of the wound with flaps (muscle or myocutaneous). Surgical debridement consisted of 2 steps. The first step was wide carcinological-like excision of the ulcer, made up of macroscopically pink tissue, with low healing potential, until reaching a healthy zone, that is, a normally vascularized tissue with no area of necrosis. The second step was to perform a resection of a bone slice on the ischium, the sacrum, or the trochanter, with a thickness of 1 or 2 mm, in order to ensure the absence of osteitis during of the ascent of the flap. Possible calcifications were also removed, as factors of recurrence of the ulcer.
Medical charts were reviewed using a standardized data set to collect demographic characteristics (age, sex, main comorbidities, risk factors), biological and microbiological data (laboratory tests, organisms identified), and outcomes of each episode at day 45 and 1 year after surgery. One patient could be included several times (for each surgery performed).
Intraoperative samples (at least 3) were performed during surgery in patients with no antibiotic treatment in the previous 15 days. Bone and soft tissue specimens were collected and sent for microbiological analysis.
Suction drainages were implanted during surgery, and removal was performed when the liquid volume was <50 cc/24 hours. Liquids from suction drainage were microbiologically analyzed.
Intraoperative samples were processed independently as previously described, with continuously monitored broth enrichment [10].
All isolates were identified by mass spectrometry (Microflex LT Mass Spectrometer, Bruker Daltonics, Bremen, Germany), and their antimicrobial susceptibility was tested by the agar disk diffusion method using the Société Française de Microbiologie (SFM) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) guidelines [11]. Minimal inhibitory concentration (MIC) tests (E-test or microdilution technique) were performed in some cases.
Criteria for microbiological identification of the causative agent were isolation in ≥1 positive intraoperative sample, except for skin bacterium (possible contaminant).
A minimum of 3 bacterial cultures was required from different samples taken during the same surgery or on different blood cultures, yielding the same pathogen (≥2 identical specimens if the pathogen was a skin bacterium, such as a coagulase-negative Staphylococcus spp., Propionibacterium acnes, or Corynebacteria, Lactobacillus, or Micrococcus spp.).
In case of various anaerobic bacteria in the same specimen, identification and antimicrobial susceptibility testing were not performed. The different microorganisms were referred to as anaerobic flora because of the global susceptibility of anaerobic bacteria to amoxicillin-acid clavulanic.
MDRO status was determined for the Enterobacteriaceae group, Acinetobacter spp., Pseudomonas aeruginosa, and Enterococcus spp. as acquired nonsusceptibility to ≥1 agent in ≥3 antimicrobial categories, and for Staphylococcus aureus as resistance to methicillin, as described by the National Committee for Clinical Laboratory Standards [12].
Confirmation of extended-spectrum β-lactamase (ESBL) activity was performed as described by the National Committee for Clinical Laboratory Standards [12, 13]. Detection of methicillin resistance for Staphylococcus aureus was performed using the disk diffusion method with cephamycin, cefoxitin, and moxalactam, and detection of the mecA gene was performed by polymerase chain reaction [14].
Systematic immediate empiric postoperative antimicrobial treatment was intravenous amoxicillin-clavulanate (2 g/125 mg 3 times daily), except in patients with contraindication or allergies, with oral switch as soon as possible (usually 2 days). In case of allergy, patients received aztreonam and clindamycin. Once the microbiological findings were received, in case of cultures from intraoperative samples positive for microorganisms not susceptible to amoxicillin-clavulanate, the antibiotic treatment was modified to an effective antibiotic treatment.
Adjustments to the antibiotic regimen were decided by a multidisciplinary team composed of an infectious disease specialist, a microbiologist, a physical and medicine and rehabilitation physiatrists, and a surgeon as soon as antibiograms were available. Drug selection by these physicians was supported by microbiological efficacy and efficient bone diffusion and was in accordance with national and international guidelines for bone and joint infections, tailored according to patient characteristics (allergy, renal function, etc.) [15, 16].
Thus, use of a combination with trimethoprim-sulfamethoxazole or fluoroquinolones was prioritized (Supplementary Table 1). Oral drugs with low bioavailability and poor bone diffusion such as cefixime, fosfomycin trometamol, and nitrofurantoin were not authorized for treatment. Oral route with high dosage was prioritized, if possible, usually when antibiotic susceptibility analyses were available.
The total duration of effective antimicrobial treatment was modified from the 10 days before January 1, 2018 (first period), to the 5 to 7 days after (second period).
All patients were followed by a multidisciplinary team for at least 1 year after surgery.
Favorable outcome was defined as the absence of all the following criteria: dehiscence, local signs of inflammation, sepsis, additional antibiotic treatment, unplanned surgery, or death due to an infectious cause.
Delay to effective antimicrobial treatment was the time period between surgical intervention and adjustment to effective antimicrobial treatment.
All continuous variables are presented as mean and standard deviation, and categorical variables are presented as number and frequency. The distributions of categorical variables were compared using chi-square tests, whereas 2-tailed, unpaired t tests were used to compare the distributions of quantitative continuous variables. A P value <.05 was considered statistically significant.
To identify risk factors associated with failure, a univariable analysis by logistic regression was performed using demographic and medical characteristics as well as all clinical and biological data. A multivariable analysis by logistic regression was then performed using all variables from the univariable analysis that had a P value ≤.05. The final model was obtained using backward stepwise regression with 0.10 thresholds. Odds ratios (ORs) were calculated from the univariate and multivariable analysis to quantify the association with failure 1 year after surgery with 95% CIs.
All analyses were performed using Statistical Package for Social Sciences (SPSS), version 26.0 (SPSS, Chicago, IL, USA).
This research was conducted in accordance with the Declaration of Helsinki and with national and institutional standards. No patient included in the study expressed opposition to the use of their clinical data in this retrospective study. This study was approved by the scientific and ethical committee of CER-MIT (IRB 00011642). This study is registered with ClinicalTrials.gov, NCT03964818, and is now complete.
RESULTS
In total, 496 patients were screened, 81 were excluded, and 415 were included (Figure 1). Our study population characteristics are described in Table 1. The mean age ± SD was 53.0 ± 14.4 years, and 77.6% were male patients.
Figure 1.
Study flowchart.
Table 1.
Study Population Characteristics
| Total (n = 415) | Cure (n = 287) | Failure (n = 128) | P Value | |
|---|---|---|---|---|
| Age, mean ± SD, y | 53.0 ± 14.4 | 52.9 ± 14.6 | 53.2 ± 14.1 | .828 |
| Male patient | 322 (77.6) | 225 (78.4) | 97 (75.8) | .513 |
| Type of spinal cord injury | ||||
| Paraplegia | 294 (70.8) | 203 (70.7) | 91 (71.1) | .981 |
| Tetraplegia | 120 (28.9) | 83 (28.9) | 37 (28.9) | .981 |
| Immunosuppression | 101 (24.3) | 63 (22.0) | 38 (29.7) | .097 |
| Diabetes mellitus | 78 (18.8) | 50 (17.4) | 28 (21.9) | .298 |
| HIV | 5 (1.2) | 4 (1.4) | 1 (0.8) | .593 |
| Solid tumor | 6 (1.4) | 3 (1.0) | 3 (2.3) | .311 |
| Hematology malignancies | 3 (0.7) | 3 (1.0) | 0 (0.0) | .244 |
| Site of pressure ulcer | ||||
| Sacrum | 134 (32.3) | 100 (34.8) | 34 (26.6) | .096 |
| Ischium | 267 (64.3) | 176 (61.3) | 91 (71.1) | .055 |
| Trochanter | 40 (9.6) | 25 (8.7) | 15 (11.7) | .338 |
| Biological analysis, mean ± SD | ||||
| White blood count, 109/L | 10.0 ± 3.7 | 9.9 ± 3.6 | 10.1 ± 4.0 | .641 |
| Neutrophil count, 109/L | 7.1 ± 3.4 | 6.9 ± 3.4 | 7.3 ± 3.5 | .453 |
| C-reactive protein level, mg/L | 51.9 ± 57.0 | 47.1 ± 52.8 | 62.9 ± 64.4 | .016* |
| Preoperative samples | ||||
| Polymicrobial | 403 (97.1) | 279 (97.2) | 124 (96.9) | .850 |
| Staphylococcus spp. | 346 (83.4) | 243 (84.7) | 103 (80.5) | .289 |
| S. aureus | 234 (56.4) | 157 (54.7) | 77 (60.2) | .301 |
| Coagulase-negative staphylococci | 191 (46.0) | 142 (49.5) | 49 (38.3) | .035* |
| Streptococcus spp. | 186 (44.8) | 125 (43.6) | 61 (47.7) | .438 |
| Enterococcus spp. | 144 (34.7) | 96 (33.4) | 48 (37.5) | .423 |
| Corynebacterium spp. | 201 (48.4) | 137 (47.7) | 64 (50.0) | .670 |
| Corynebacterium striatum | 177 (42.7) | 120 (41.8) | 57 (44.5) | .605 |
| Enterobacterales | 267 (64.3) | 188 (65.5) | 79 (61.8) | .457 |
| Escherichia coli | 155 (37.3) | 112 (39.0) | 43 (33.6) | .291 |
| Enterobacter spp. | 19 (4.6) | 13 (4.5) | 6 (4.7) | .943 |
| Morganella morganii | 35 (8.4) | 25 (8.7) | 10 (7.8) | .761 |
| Proteus spp. | 114 (27.5) | 79 (27.5) | 35 (27.3) | .969 |
| Klebsiella spp. | 72 (17.3) | 49 (17.1) | 23 (17.9) | .824 |
| Citrobacter spp. | 18 (4.3) | 15 (5.2) | 3 (2.3) | .183 |
| Pseudomonas aeruginosa | 43 (10.4) | 28 (9.8) | 15 (11.7) | .545 |
| Acinetobacter spp. | 14 (3.4) | 8 (2.8) | 6 (7.0) | .322 |
| Anaerobes | 110 (26.5) | 73 (25.4) | 37 (28.9) | .459 |
| Candida spp. | 5 (1.2) | 2 (0.7) | 3 (2.3) | .173 |
| Presence of MDRO | 86 (20.7) | 55 (19.2) | 31 (24.2) | .241 |
| MRSA | 66 (15.9) | 43 (15.0) | 23 (18.0) | .431 |
| ESBL | 23 (5.5) | 14 (4.8) | 9 (7.0) | .370 |
| Suction drainage samples | ||||
| Positive samples | 199 (48.0) | 128 (44.6) | 71 (55.5) | .049* |
| Antibiotic treatment | ||||
| Immediate effective empiric treatment | 219 (52.8) | 161 (56.1) | 58 (45.3) | .042* |
| Primary outcome (at 1 y) | ||||
| Duration of effective treatment 5–7 d | 235 (56.6) | 169 (71.9) | 66 (28.1) | .153 |
| Duration of effective treatment 10 d | 179 (43.1) | 117 (65.3) | 62 (34.6) |
Data are presented as No. (%), unless otherwise indicated.
Abbreviations: ESBL, extended-spectrum β-lactamase; MDRO, multidrug-resistant organism; MRSA, methicillin-resistant Staphylococcus aureus.
Statistically significant.
The main microorganisms identified were Enterobacterales (n = 267; 64.3%), Staphylococcus aureus (n = 234; 56.4%), and coagulase-negative staphylococci (n = 191; 46.0%). Multidrug-resistant organisms (MDROs) were involved in 86 (20.7%) cases, including 66 (15.9%) cases with methicillin-resistant S. aureus (MRSA) and 23 (5.5%) cases with ESBL-producing Enterobacterales (ESBL-E).
Favorable outcomes were recorded in 287 (69.2%) cases within 1 year follow-up. Failure was due to dehiscence (n = 110; 38.3%), additional surgery (n = 88; 30.7%), local signs of inflammation (n = 37; 12.9%), sepsis (n = 12; 4.2%), death due to infectious disease (n = 8; 2.8%), and additional antibiotic treatment without surgery (n = 7; 2.4%).
The mean delay before effective antibiotic treatment was 4.8 ± 1.9 days. All effective antibiotic prescriptions are reported in Supplementary Table 1
Overall, 235 (56.6%) patients were treated for 5 to 7 days, and 179 (43.1%) patients were treated for 10 days. The epidemiological, clinical, and biological population characteristics between these 2 groups were not significantly different (Supplementary Table 2). The cure rate was not significantly different between these 2 treatment durations: 79.1% vs 83.2% (P = .315) within 45 days and 71.9% vs 65.3% (P = .153) at 1-year follow-up in the 5–7-day treatment group and 10-day treatment group, respectively. Failure rates during follow-up according to immediate or delayed effective antibiotic treatment or antibiotic treatment durations are presented in Supplementary Figure 1.
The univariable and multivariable analyses are presented in Table 2.
Table 2.
Risk Factors for Failure on Univariable and Multivariable Analyses
| Univariable Analysis | Multivariable Analysis | |||
|---|---|---|---|---|
| Variable | Odds Ratio [95% CI] | P Value | Odds Ratio [95% CI] | P Value |
| Coagulase-negative staphylococci | 0.633 [0.414–0.969] | .035 | 0.617 [0.384–0.991] | .046 |
| Positive culture from suction drainage | 1.531 [1.000–2.342] | .050 | 1.622 [1.005–2.617] | .048 |
| C-reactive protein level >52 mg/L | 1.697 [1.062–2.711] | .027 | 1.570 [0.967–2.548] | .068 |
| Immediate effective empiric antibiotic treatment | 0.648 [0.427–0.986] | .043 | … | … |
In the multivariate analysis, the only risk factor associated with failure was a positive culture from suction drainage (odds ratio [OR], 1.622; 95% CI, 1.005–2.617; P = .046), while intraoperative samples positive for coagulase-negative staphylococci were associated with cure (OR, 0.617; 95% CI, 0.384–0.991; P = .046).
Furthermore, patients with a 5–7-day treatment duration and delay before effective antimicrobial treatment did not have a significantly higher risk of failure than patients with immediate effective antibiotic treatment and 10-day treatment duration (72.8% vs 66.7%; P = .371). Finally, intraoperative samples positive for MDROs were not associated with worse outcomes (19.2% vs 24.2%; P = .241).
DISCUSSION
We present a large cohort of perineal presumed osteomyelitis associated with pressure ulcers managed by a standardized strategy: surgery with excision of the infected tissues and bone shaving, followed by coverage of the tissue loss and short antibiotic treatment.
In the literature, surgical complications and recurrences during management of pressure ulcers are frequent and vary from 21% to 79% [17, 18].
The main bacteria identified in pressure ulcers in our study are similar to those found in the literature, with a majority being Staphylococcus spp. and Streptococcus spp. [19], while Enterobacterales are similarly commonly encountered [20–25]. We also have a high rate of polymicrobial infections, as often described [25]. Finally, we have a high number of infections due to MDROs with MRSA and ESBL-E, which is in line with the high proportion of MDRO carriage and infection in the population of SCI patients [26, 27]. It should be noted that the presence of MDROs was not associated with worse outcomes in our study.
Regarding therapeutic management for osteomyelitis in perineal pressure ulcers, data are limited in the literature. A combined medical and surgical approach with wound coverage seems more effective, with a higher cure rate than antibiotic therapy alone [19, 21, 28, 29].
The optimal antibiotic treatment duration is unknown, and data are very scarce. In our study, a very short treatment duration of 5–7 days seemed sufficient. This could be due to the physiopathology of the infection, type of bone tissue involved (spongy bone), or secondary revascularization of the diseased bone due to a covering muscle and cutaneous flap.
Several studies did not find a benefit of long treatment duration (>3 weeks) vs short treatment duration (≤7 days) if the surgical procedure was satisfactory [23, 29, 30].
Moreover, immediate postoperative empiric antimicrobial treatment was microbiologically ineffective in 47.2%, yet a delay before prescription of effective treatment was not associated with lower cure rate in our multivariable analysis. Also, patients with a delay to effective antibiotic treatment and a treatment duration of 5–7 days did not have significantly worse outcomes, and treatment duration was not correlated with favorable outcomes.
In our study, we evaluated a short and nontraditional duration of antimicrobial therapy with early oral switch during osteomyelitis due to pressure ulcers, which is counter to the current dogma in infectious disease [31]. A randomized controlled trial is warranted [9].
In our study, a positive culture of fluid from suction drainage was associated with a higher failure rate. These data have been studied in prosthetic joint infections (PJIs), and positive cultures from suction drainage were associated with high positive predictive value for failure [32]. We can therefore hypothesize that positive cultures from suction drainage reflect the residual bacterial inoculum and indicate that surgical debridement and bone shaving were insufficient.
Several limitations could be raised, such as the retrospective design and its inherent bias, as well as the monocentric design. However, this meant that all patients were operated on by the same surgical team, and the management was homogenous. Finally, we were not able to perform histology of the exposed bone, as this is not part of our standard of care, but the presence of microorganisms in intraoperative samples clearly suggested infection.
CONCLUSIONS
Management of presumed osteomyelitis-complicating pressure ulcers with large surgical debridement, bone shaving, and covering with musculo-tendinous flaps, followed by a short antibiotic treatment of 5–7 days, seems safe and effective.
The role of antibiotics in disease management still needs to be defined after appropriate surgery, which is a major concern in this population with high incidence of MDRO infection. The only factor associated with failure was positive culture from suction drainage.
More data are warranted on this specific problem, especially through randomized controlled trials, and prevention through adequate monitoring for possible risk factors for pressure ulcers in this frail population is of utmost importance.
Supplementary Material
Contributor Information
Aurélien Dinh, Infectious Disease Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Emma D’anglejan, Infectious Disease Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Helene Leliepvre, Physical Medicine and Rehabilitation, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Frédérique Bouchand, Pharmacy, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Damien Marmouset, Orthopaedics Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Nathalie Dournon, Infectious Disease Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Hélène Mascitti, Infectious Disease Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
François Genet, Physical Medicine and Rehabilitation, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Jean-Louis Herrmann, Microbiological Laboratory, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Haude Chaussard, Orthopaedics Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Clara Duran, Infectious Disease Department, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Latifa Noussair, Microbiological Laboratory, University Hospital Raymond-Poincaré, APHP Paris Saclay, Versailles Saint Quentin University, Garches, France.
Supplementary Data
Supplementary materials are available at Open Forum Infectious Diseases online. Consisting of data provided by the authors to benefit the reader, the posted materials are not copyedited and are the sole responsibility of the authors, so questions or comments should be addressed to the corresponding author.
Acknowledgments
Financial support. No external funding was received.
Potential conflicts of interest. The authors declare no conflicts of interest. Co-authors affiliated with the funding agency facilitated the funding process and the provision of study material. They were involved in the study design, data collection, and data interpretation under the leadership of an independent principal investigator from the DRC Ministry of Health. The views expressed in this work do not reflect JICA's opinion.
Author contributions. A.D. developed the study design. J.L.H. and L.N. performed all laboratory tests. E.D., C.D., and L.N. were responsible for data collection. A.D. and C.D. performed the statistical analysis. A.D., F.B., and C.D. were responsible for data analysis and data interpretation. A.D., E.D., F.B., C.D., and L.N. drafted the first version of the manuscript. All authors revised and approved the final manuscript.
Patient consent. The research was conducted in accordance with the Declaration of Helsinki and national and institutional standards. No patient included in the study expressed opposition to the use of clinical data in this retrospective study.
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