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Risk Factor Analysis of Deep Surgical Site Infection After Posterior Instrumented Fusion Surgery for Spinal Trauma: A Multicenter Observational Study
Original Article
Risk Factor Analysis of Deep Surgical Site Infection After Posterior Instrumented Fusion Surgery for Spinal Trauma: A Multicenter Observational Study Satoshi Ogihara1, Takashi Yamazaki3, Michio Shiibashi2, Toru Maruyama4, Hirotaka Chikuda5, Kota Miyoshi6, Hirohiko Inanami7, Yasushi Oshima8, Seiichi Azuma9, Naohiro Kawamura10, Kiyofumi Yamakawa11, Nobuhiro Hara3, Jiro Morii12, Rentaro Okazaki9, Yujiro Takeshita6, Kei Sato1, Sakae Tanaka8, Kazuo Saita1
BACKGROUND: Surgical site infection (SSI) is a dire complication in spinal surgeries, resulting in reoperation, prolonged hospitalization, and increased expenses. Patients with traumatized spine have been reported to have a high risk of postoperative SSI. Precise identification of risk factors associated with SSI can be helpful in its prevention. However, there are only a limited number of studies investigating risk factors of SSI after posterior instrumented fusion for traumatized spine.
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METHODS: From July 2010 to June 2015, we conducted an observational study on deep SSI after posterior instrumented fusion surgery for spinal trauma in adult patients at 10 research hospitals. Detailed clinical data were prospectively collected using a standardized data collection chart and were retrospectively analyzed. SSI was diagnosed based on the definition by the Centers for Disease Control and Prevention.
CONCLUSIONS: The complexity of patients and resident involvement in surgeries may be greater at academic than at nonacademic hospitals. ASA score can be considered as an accessible and comprehensive tool for surgeons to preoperatively gauge the potential risk of SSI, a complex clinical entity. The results of this study can improve clinicians' risk perception in those undergoing posterior fusion for spinal trauma.
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RESULTS: A total of 623 consecutive adult patients were enrolled in this study, of which 20 (3.2%) developed deep SSI. According to multivariate regression analysis, surgery at academic hospitals (P [ 0.004) and an American Society of Anesthesiologists (ASA) score ‡3 (P [ 0.017) were independent predictors of deep SSI after posterior instrumented fusion surgery for spinal trauma.
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Key words - American Society of Anesthesiologists - Instrumentation - Posterior fusion - Risk factor - Spinal trauma - Surgical site infection Abbreviations and Acronyms ASA: American Society of Anesthesiologists MI: Minimally invasive SSI: Surgical site infection From the 1Department of Orthopaedic Surgery and 2Information Technology Center, Saitama Medical University, Saitama; Departments of Orthopaedic Surgery, 3Musashino Red Cross
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INTRODUCTION
S
urgical site infection (SSI) is a threatening postoperative complication in spinal surgeries because it can result in reoperation (washing and surgical debridement), prolonged hospital stays, and increased expenses. Spinal trauma is a unique pathologic condition considered for spinal surgery, and the number of patients who undergo this surgery is smaller than those undergoing surgery for degenerative spinal diseases. Previously, spinal trauma was reported as an independent risk factor for postoperative SSI in the literature.1,2 The development of spinal instrumentation provided immediate stability for unstable traumatized spine with fractures and/or dislocations and may have facilitated early bed leaving, start of rehabilitation, and decreased incidence of complications associated with prolonged bed rest, such as pressure skin ulcers, deep vein thrombosis,
Hospital, Tokyo, 4Saitama Rehabilitation Center, Saitama, 5Faculty of Medicine, Gunma University, Gunma, 6Yokohama Rosai Hospital, Kanagawa, 7Iwai Orthopaedic Medical Hospital, Tokyo, 8Faculty of Medicine, University of Tokyo, Tokyo and 9Saitama Red Cross Hospital, Saitama; 10Department of Spine and Orthopaedic Surgery, Japanese Red Cross Medical Center, Tokyo; 11Department of Orthopaedic Surgery and Musculoskeletal Oncology, Tokyo Metropolitan Komagome Hospital, Tokyo; and 12Department of Orthopaedic Surgery, Sanraku Hospital, Tokyo, Japan To whom correspondence should be addressed: Satoshi Ogihara, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.10.117 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
pulmonary embolism, and pneumonia.3 On the contrary, several reports described the use of spinal instrumentation as an independent risk factor for SSI in spinal surgeries,4,5 especially in case of posterior surgery.4,5 Spinal trauma and the concurrent use of posterior spinal instrumentation can be suspected to cumulatively increase the risk of SSI after spinal surgery. However, at present, there are only a limited number of reports that have investigated the risk factors for SSI after posterior instrumented fusion surgery for traumatized spine. The aim of this study was to determine the precise independent risk factors in adult patients for deep SSI after posterior instrumented fusion surgery for spinal trauma. In this study, we have retrospectively reviewed prospectively collected multicenter observational research data of 623 registered cases. PATIENTS AND METHODS Study Design and Selection Criteria This observational study was conducted from July 1, 2010, to June 30, 2015, involving 10 hospitals in Japan, with a minimum of 12 months of postoperative follow-up for each of the enrolled cases. This study was approved by the institutional review boards of Saitama Medical University, Musashino Red Cross Hospital, University of Tokyo, Sagamihara National Hospital, Saitama Red Cross Hospital, Japanese Red Cross Medical Center, Tokyo Metropolitan Komagome Hospital, Sanraku Hospital, Yokohama Rosai Hospital, and Iwai Orthopedic Medical Hospital. Given the observational nature of this study, the requirement for written consent from the study subjects was waived by the institutional review boards of the participating hospitals. Information for opt-out was posted on the website of Saitama Medical University. The prospectively collected clinical data from the participating hospitals were anonymized and deidentified prior to the analyses. Detailed preoperative and operative patient characteristics were recorded prospectively using a standardized data collection chart. In this study, spinal trauma was defined as spinal fracture and/or dislocation, and cases with pathologic spinal fracture such as tumoral or infectious spinal abnormalities were excluded. Patients included in this study had undergone conventional posterior open instrumented surgery; however, patients who had undergone minimally invasive (MI) surgery with percutaneous pedicle screws were excluded. Patients <18 years and/or who had undergone single-stage anterior-posterior surgery were also excluded. The SSI definition according to the Centers for Disease Control and Prevention6 was used by the participating hospitals, and wound infection that occurred within 12 months of hardware implantation involving the deep soft tissues was considered as deep SSI.6 Data Collection The prospectively obtained preoperative patient characteristics included age at the time of surgery, sex, height, and weight. Preoperative patient-related risk factors of SSI included smoking, diabetes mellitus, body mass index, American Society of Anesthesiologists (ASA) score,7 and preoperative chronic steroid use. Additionally, data of surgery-related factors including operation duration, intraoperative blood loss, anatomic location of the surgery (cervical, thoracic, and/or lumbosacral), emergency surgery, dural tear, use of intraoperative fluoroscopy, use of a bioclean
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room, prophylactic intravenous administration of cefazolin, intrawound administration of powdered vancomycin, and type (academic or nonacademic) of hospital, considered as possible risk factors for SSI, were collected and analyzed. The microbiological culture results from all patients with deep SSI were recorded and assessed. In patients who underwent open debridement, microbial cultures were analyzed to confirm the development of SSI and to determine the subsequent course of treatment. Statistical Analysis The associations between deep SSI and potential risk factors were analyzed. Fisher exact test and Student t test were used for categorical and continuous variables, respectively. Multivariate analysis was performed to evaluate the risk factors of SSI. The significant variables and the variables that correlated (P < 0.20) with SSI in univariate analysis were entered into a stepwise multiple logistic regression model. Statistical analysis was performed using SPSS Statistics version 24 (IBM Corp., Armonk, New York, USA). P ¼ 0.05 was considered statistically significant. RESULTS From July 2010 to June 2015, a total of 623 consecutive patients (292 women and 331 men; mean age, 63.0 years; age range, 18e97 years) from 10 hospitals in Japan were enrolled for this study. Overall, 20 patients (3.2%) developed postoperative deep SSI. The demographic characteristics of the patients included in this study are given in Table 1. With respect to the demographic characteristics, surgery at academic hospitals and ASA score 3 were significantly associated with SSI (P < 0.05), whereas age 61 years, preoperative chronic steroid use, and dural tear were correlated (P < 0.20) with SSI. These results are similar to those obtained from the univariate logistic regression analysis (Table 2). Table 3 shows the results of the multivariate logistic regression analysis, including the variables that correlated with SSI (P < 0.20) in the univariate logistic regression analysis. The results confirmed that surgeries at academic hospitals (P ¼ 0.004; odds ratio, 4.13; 95% confidence interval, 1.58e10.85) and ASA score 3 (P ¼ 0.017; odds ratio, 3.10; 95% confidence interval, 1.22e7.88) were independent predictors of SSI, whereas advanced age (61 years) tended to correlate with risk of SSI (P ¼ 0.077). Microbial cultures were constantly obtained for testing in the 20 patients who had developed deep SSI, and 80.0% of these patients (16 of 20) had a positive culture with a single organism. Staphylococcus aureus was present in 56.3% of the positive cultures (9 of 16), of which 55.6% (5 of 9) were methicillin-resistant S. aureus. Coagulase-negative staphylococci and Pseudomonas aeruginosa were the next most common organisms, both occurring in 12.5% of the positive cultures (2 of 16) (Table 4). DISCUSSION In this study, we sought to identify the independent risk factors in adult patients susceptible to deep SSI after posterior instrumented fusion surgery for spinal trauma. The number of previous studies on SSI after surgeries for spinal trauma is very limited.8-12 This may be because the number of patients who undergo surgeries for
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ORIGINAL ARTICLE SATOSHI OGIHARA ET AL.
SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
Table 1. Demographic Characteristics of the Surgical Site Infection and NoneSurgical Site Infection Groups SSI Group (n [ 20)
Non-SSI Group (n [ 603)
P Value
67.5 18.0
62.8 20.0
0.292
Age 61 years
17 (85.0)
397 (65.8)
0.055
Men
9 (45.0)
322 (53.4)
0.303
22.3 3.3
22.6 3.8
0.761
ASA score 3
8 (40.0)
115 (19.1)
0.028
Diabetes mellitus
3 (15.0)
73 (12.1)
0.449
Characteristics Age (years)
2
Body mass index (kg/m )
Hemodialysis
1 (5.0)
8 (1.32)
0.256
Smoking
2 (10.0)
58 (9.62)
0.591
Preoperative chronic steroid use
3 (15.0)
36 (5.97)
0.123
3 (15.0)
115 (19.1)
0.457
Anatomic location of the surgery Surgery including cervical spine Surgery including thoracic spine
11 (55.0)
329 (54.6)
0.577
Surgery including lumbosacral spine
15 (75.0)
446 (74.0)
0.577
Dural tear
3 (15.0)
42 (7.0)
0.169
Use of an intraoperative fluoroscopy
5 (25.0)
199 (33.0)
0.313
Use of a bioclean room
5 (25.0)
163 (27.0)
0.537
Emergency surgery
5 (25.0)
168 (27.9)
0.504
Operative time (minutes)
213.3 56.3
216.0 92.0
0.839
Intraoperative bleeding (mL)
409.8 529.6
610.1 721.7
0.219
Prophylactic intravenous administration of CEZ
17 (85.0)
550 (91.2)
0.265
Intrawound application of vancomycin powder
4 (20.0)
143 (23.7)
0.471
Surgery at academic hospitals
7 (35.0)
75 (12.4)
0.010
Values are number of patients (%), mean SD, or as otherwise indicated. SSI, surgical site infection; ASA, American Society of Anesthesiologists; CEZ, cefazolin.
spinal trauma is lower. Dubory et al.,11 in a case series of prospectively collected 518 patients with spinal injuries (including anterior and/or posterior procedures), reported a 4. 8% rate of SSI. Cooper et al.12 reported an infection rate of 4. 0% in a retrospective review of 358 patients who underwent instrumented fixation for spinal trauma (including anterior and/ or posterior procedures). In this study, the registered number of cases from multiple centers was 623; to our knowledge, it is the largest sample size to be prospectively collected for posterior instrumented fusion in spinal trauma. In this study, the incidence of deep SSI was 3.2%, which is considered to be a relatively favorable SSI rate in the case of spinal injury.8-12 It has been reported that superficial SSI is difficult to precisely distinguish from delayed wound healing13; therefore, as an accurate definition of wound infection, only deep SSI was investigated in this study. Accordingly, the infection rate may have been lower because of the exclusion of superficial SSI. In this analysis, surgery at academic hospitals was identified as an independent predictor of development of deep SSI. Although a definitive explanation for the increased risk of SSI at academic hospitals may be difficult to deduce from our data alone, several
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characteristics of academic hospitals are speculated as the cause of this increase. First, the academic hospitals participating in this study were all tertiary care referral institutions, and might have encountered more complex spinal trauma cases than nonacademic hospitals. Second, resident education is inherent to the mission of academic hospitals. Schoenfeld et al.14 reported that resident involvement is correlated with higher risk of SSI after spinal arthrodesis in a retrospective review of the American College of Surgeons' National Surgical Quality Improvement Program database. In contrast, Phan et al.15 found that resident participation in cervical and lumbar spine surgeries did not increase complication rates in their multicenter retrospective cohort. In addition, as a consequence of medical student and resident education at academic hospitals, there is a possibility that the number of people in operating rooms and the frequency of door opening may be increased. There are several reports showing that an increased number of people in the operating room is associated with the incidence of SSI,16-18 and that increased door opening frequency is associated with high air bacterial counts in the operating room.18-20 A precise cause for the difference in the SSI rate between academic and nonacademic hospitals observed in our study could not
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
Table 2. Univariate Logistic Regression Analysis for Deep Surgical Site Infection After Posterior Instrumented Fusion for Spinal Trauma Characteristics
OR (95% CI)
P Value
Age 61 years
2.94 (0.85e10.14)
0.088
Male sex
0.714 (0.292e1.748)
0.461
Body mass index
0.981 (0.870e1.107)
0.760
ASA score 3
2.829 (1.130e7.080)
0.026
Diabetes mellitus
1.281 (0.367e4.479)
0.698
Hemodialysis
3.914 (0.466e32.889)
0.209
Smoking
1.044 (0.236e4.613)
0.955
Preoperative chronic steroid use
2.779 (0.778e9.925)
0.115
Surgery including cervical spine
0.749 (0.216e2.598)
0.649
Surgery including thoracic spine
1.018 (0.416e2.492)
0.969
Surgery including lumbosacral spine
Anatomic location of the surgery
1.056 (0.378e2.953)
0.917
Dural tear
2.357 (0.664e8.367)
0.185
Use of an intraoperative fluoroscopy
0.677 (0.242e1.888)
0.456
Use of a bioclean room
0.900 (0.322e2.515)
0.840
Emergency surgery
0.863 (0.309e2.412)
0.779
Operative time
1.000 (0.995e1.005)
0.896
Intraoperative bleeding
0.999 (0.998e1.000)
0.222
Prophylactic intravenous administration of CEZ
0.546 (0.155e1.924)
0.346
Intrawound application of vancomycin powder
0.804 (0.265e2.444)
0.701
Surgery at academic hospitals
3.791 (1.466e9.803)
0.006
OR, odds ratio; CI, confidence interval; ASA, American Society of Anesthesiologists; CEZ, cefazolin.
be determined; however, the aforementioned factors may correlate with an increased risk of wound infection. An ASA score 3 was also found to be significantly associated with an increased risk of deep SSI in our multivariate analysis. Lonjon et al.10 reported that ASA score was a significant predictor of risk during early (3 months) SSI after surgery for traumatized spine, and there have been several studies that have identified
Table 3. Multivariate Logistic Regression Analysis for Deep Surgical Site Infection After Posterior Instrumented Fusion for Spinal Trauma Characteristic
OR (95% CI)
Age 61 years
P Value 0.077
ASA score 3
3.10 (1.22e7.88)
0.017
Preoperative chronic steroid use
0.131
Dural tear
0.153
Surgery at academic hospitals
4.13 (1.58e10.85)
0.004
OR, odds ratio; CI, confidence interval; ASA, American Society of Anesthesiologists.
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ASA score as being independently associated with the incidence of SSI after elective spinal surgeries.4,5,21 The result of this study is consistent with those of previous studies that have described higher ASA scores as a significant predictor for SSI. ASA score was originally developed to preoperatively assess the overall physical status of the patient.6 ASA score is a reliable index for the evaluation of preoperative general condition, and the ASA classification has been reported to achieve 98% reliability (þ1 class) across different anesthesiologists.22 Spinal trauma is a complex clinical entity; however, ASA score can be a relatively accessible and comprehensive indicator of SSI risk. Multivariate analysis of this study revealed that advanced age (61 years) had the tendency to be associated with be an independent risk factor (P ¼ 0.077), similar to that reported by Dubory et al.11 in their case series. Spinal trauma includes the 2 following categories: vertebral fracture without osteoporosis because of high energy injury such as traffic accident or fall from high places, and osteoporotic vertebral fracture because of low energy injury. In this study, the patients were not distinguished according to these categories. However, elderly patients with a high incidence of SSI in our data may have the clinical characteristic of the latter category of spinal trauma. A single-institutional retrospective study described patients with
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
Table 4. Microbiological Characteristics of Surgical Site Infection Organisms
Number of Cases
MRSA
5
Methicillin-sensitive Staphylococcus aureus
4
Pseudomonas aeruginosa
2
Methicillin-resistant CoNS
1
CoNS
1
Enterobacter cloacae
1
Citrobacter koseri
1
Serratia marcescens
1
Unknown
4
MRSA, methicillin-resistant S aureus; CoNS, coagulase-negative staphylococci.
osteoporosis as having an increased SSI risk in lumbar elective surgeries.23 Additionally, patients with osteoporotic vertebral fracture are reported to have a statistically significant higher implant removal rate than patients with degenerative disease with SSI after instrumented fusion,24 and there is a previous report that has described cases with osteoporotic vertebral fracture as at a high risk of death from infectious diseases.25 From these previous reports, an association between osteoporotic vertebral fracture and susceptibility to infections is inferred. Kobayashi et al.26 reported that the need for surgery for osteoporotic vertebral fractures has increased in recent periods; accordingly, the association between osteoporosis vertebral fracture and SSI risk is a noteworthy research topic. To precisely investigate the relationship between advanced age, osteoporotic vertebral fractures, and SSI after fusion surgery for spinal trauma, additional research with a prospective study design and large sample size is needed. This study has several limitations. First, the number of patients who developed SSI was relatively small (n ¼ 20), given that only those patients with deep SSI (excluding superficial SSI) after specific types of procedures (posterior instrumented fusion surgery for spinal trauma) were included. Second, this study did not account
REFERENCES 1. Watanabe M, Sakai D, Matsuyama D, Yamamoto Y, Sato M, Mochida J. Risk factors for surgical site infection following spine surgery: efficacy of intraoperative saline irrigation. J Neurosurg Spine. 2010;12:540-546. 2. Ogihara S, Yamazaki T, Maruyama T, et al. Prospective multicenter surveillance and risk factor analysis of deep surgical site infection after posterior thoracic and/or lumbar spinal surgery in adults. J Orthop Sci. 2015;20:71-77. 3. Rea G, Zerick W. The treatment of thoracolumbar fractures: one point of view. J Spinal Disord. 1995;8: 368-382.
for several previously studied factors associated with spinal trauma, including the number of operated levels,9-11 preoperative neurologic deficit (American Spinal Injury Association grade),11 polytrauma (injury of other organs),11,12 and timing of surgery after admission.9-11 Additionally, we had not distinguished the patients as 2 categories of vertebral fractures, without osteoporosis because of high energy injury and osteoporotic vertebral fracture because of low energy injury, which might have an effect on clinical features after posterior instrumented fusion. Furthermore, patients who had undergone MI surgery with percutaneous pedicle screws were excluded to maintain a homogenous study population. However, several studies have shown a lower SSI incidence after MI transforaminal interbody fusion using percutaneous pedicle screws than after open transforaminal interbody fusion for degenerative diseases.27,28 MI surgery may reduce iatrogenic tissue injury, intraoperative bleeding, and the exposure of the operative wound to bacteria. The impact of MI fusion with percutaneous pedicle screws for spinal trauma on the incidence of SSI could be a subject of further study. The strengths of this study are the relatively large number of surgical procedures and the prospective multicenter research design that allowed for multivariate logistic regression analysis of the detailed data for the potential risk factors of SSI after spinal surgery. CONCLUSIONS We identified that surgery at academic hospitals and ASA score 3 were significantly and independently associated with the occurrence of deep SSI after posterior instrumented fusion surgery for spinal trauma in adult patients. The complexity of patients and resident involvement in surgeries may be greater at academic hospitals than nonacademic hospitals. ASA score can be a comprehensive and accessible tool for surgeons to preoperatively gauge the potential risk of SSI in patients suffering spinal trauma, a complex clinical entity. The result of this study can provide clinicians with improved risk perception when managing patients undergoing posterior fusion for spinal trauma.
ACKNOWLEDGMENTS The authors thank all the spine surgeons of the participating hospitals who supported the surgeries and data collection.
4. Maragakis LL, Cosgrove SE, Martinez EA, Tucker MG, Cohen DB, Perl TM. Intraoperative fraction of inspired oxygen is a modifiable risk factor for surgical site infection after spinal surgery. Anesthesiology. 2009;110:556-562. 5. Veeravagu A, Patil CG, Lad SP, Boakye M. Risk factors for postoperative spinal wound infections after spinal decompression and fusion surgeries. Spine (Phila Pa 1976). 2009;34:1869-1872. 6. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol. 1999;20:250-278.
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7. Owens WD, Felts JA, Spitznagel EL Jr. ASA physical status classifications: a study of consistency of ratings. Anesthesiology. 1978;49:239-243. 8. Rechtine GR, Bono PL, Cahill D, Bolesta MJ, Chrin AM. Postoperative wound infection after instrumentation of thoracic and lumbar fractures. J Orthop Trauma. 2001;15:566-569. 9. Blam OG, Vaccaro AR, Vanichkachorn JS, et al. Risk factors for surgical site infection in the patient with spinal injury. Spine (Phila Pa 1976). 2003; 28:1475-1480. 10. Lonjon G, Dauzac C, Fourniols E, et al. Early surgical site infections in adult spinal trauma: a prospective, multicentre study of infection rates
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and risk factors. Orthop Traumatol Surg Res. 2012;98: 788-794. 11. Dubory A, Giorgi H, Walter A, et al. Surgical-site infection in spinal injury: incidence and risk factors in a prospective cohort of 518 patients. Eur Spine J. 2015;24:543-554. 12. Cooper K, Glenn CA, Martin M, Stoner J, Li J, Puckett T. Risk factors for surgical site infection after instrumented fixation in spine trauma. J Clin Neurosci. 2016;23:123-127. 13. Kao LS, Ghaferi AA, Ko CY, Dimick JB. Reliability of superficial surgical site infections as a hospital quality measure. J Am Coll Surg. 2011;213:231-235. 14. Schoenfeld AJ, Carey PA, Cleveland AW III, Bader JO, Bono CM. Patient factors, comorbidities, and surgical characteristics that increase mortality and complication risk after spinal arthrodesis: a prognostic study based on 5,887 patients. Spine J. 2013;13:1171-1179. 15. Phan K, Phan P, Stratton A, Kingwell S, Hoda M, Wai E. Impact of resident involvement on cervical and lumbar spine surgery outcomes [e-pub ahead of print]. Spine J https://doi.org/10.1016/j.spinee. 2019.07.006, accessed September 30, 2019. 16. Koutsoumbelis S, Hughes AP, Girardi FP, et al. Risk factors for postoperative infection following posterior lumbar instrumented arthrodesis. J Bone Joint Surg Am. 2011;93:1627-1633. 17. Wathen C, Kshettry VR, Krishnaney A, et al. The association between operating room personnel and turnover with surgical site infection in more than 12 000 neurosurgical cases. Neurosurgery. 2016;79:889-894.
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18. Birgand G, Saliou P, Lucet JC. Influence of staff behavior on infectious risk in operating rooms: what is the evidence? Infect Control Hosp Epidemiol. 2015;36:93-106.
26. Kobayashi K, Ando K, Nishida Y, Ishiguro N, Imagama S. Epidemiological trends in spine surgery over 10 years in a multicenter database. Eur Spine J. 2018;27:1698-1703.
19. Andersson AE, Bergh I, Karlsson J, Eriksson BI, Nilsson K. Traffic flow in the operating room: an explorative and descriptive study on air quality during orthopedic trauma implant surgery. Am J Infect Control. 2012;40:750-755.
27. Parker SL, Adogwa O, Witham TF, Aaronson OS, Cheng J, McGirt MJ. Post-operative infection after minimally invasive versus open transforaminal lumbar interbody fusion (TLIF): literature review and cost analysis. Minim Invasive Neurosurg. 2011;54: 33-37.
20. Scaltriti S, Cencetti S, Rovesti S, Marchesi I, Bargellini A, Borella P. Risk factors for particulate and microbial contamination of air in operating theatres. J Hosp Infect. 2007;66:320-326. 21. Gruskay J, Kepler C, Smith J, Radcliff K, Vaccaro A. Is surgical case order associated with increased infection rate after spine surgery? Spine (Phila Pa 1976). 2012;37:1170-1174. 22. Sankar A, Johnson SR, Beattie WS, Tait G, Wijeysundera DN. Reliability of the American Society of Anesthesiologists physical status scale in clinical practice. Br J Anaesth. 2014;113:424-432.
28. Phan K, Rao PJ, Kam AC, Mobbs RJ. Minimally invasive versus open transforaminal lumbar interbody fusion for treatment of degenerative lumbar disease: systematic review and metaanalysis. Eur Spine J. 2015;4:1017-1030.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
23. Lai Q, Song Q, Guo R, et al. Risk factors for acute surgical site infections after lumbar surgery: a retrospective study. J Orthop Surg Res. 2017;12:116.
Received 2 August 2019; accepted 19 October 2019
24. Ishii M, Iwasaki M, Ohwada T, et al. Postoperative deep surgical-site infection after instrumented spinal surgery: a multicenter study. Global Spine J. 2013;3:95-102.
Journal homepage: www.journals.elsevier.com/worldneurosurgery
25. Chen YC, Lin WC. Risk of long-term infectionrelated death in clinical osteoporotic vertebral fractures: a hospital-based analysis. PLoS One. 2017;12:e0182614.
Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.10.117
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.10.117
Risk Factor Analysis of Deep Surgical Site Infection After Posterior Instrumented Fusion Surgery for Spinal Trauma: A Multicenter Observational Study Satoshi Ogihara1, Takashi Yamazaki3, Michio Shiibashi2, Toru Maruyama4, Hirotaka Chikuda5, Kota Miyoshi6, Hirohiko Inanami7, Yasushi Oshima8, Seiichi Azuma9, Naohiro Kawamura10, Kiyofumi Yamakawa11, Nobuhiro Hara3, Jiro Morii12, Rentaro Okazaki9, Yujiro Takeshita6, Kei Sato1, Sakae Tanaka8, Kazuo Saita1
BACKGROUND: Surgical site infection (SSI) is a dire complication in spinal surgeries, resulting in reoperation, prolonged hospitalization, and increased expenses. Patients with traumatized spine have been reported to have a high risk of postoperative SSI. Precise identification of risk factors associated with SSI can be helpful in its prevention. However, there are only a limited number of studies investigating risk factors of SSI after posterior instrumented fusion for traumatized spine.
-
METHODS: From July 2010 to June 2015, we conducted an observational study on deep SSI after posterior instrumented fusion surgery for spinal trauma in adult patients at 10 research hospitals. Detailed clinical data were prospectively collected using a standardized data collection chart and were retrospectively analyzed. SSI was diagnosed based on the definition by the Centers for Disease Control and Prevention.
CONCLUSIONS: The complexity of patients and resident involvement in surgeries may be greater at academic than at nonacademic hospitals. ASA score can be considered as an accessible and comprehensive tool for surgeons to preoperatively gauge the potential risk of SSI, a complex clinical entity. The results of this study can improve clinicians' risk perception in those undergoing posterior fusion for spinal trauma.
-
-
RESULTS: A total of 623 consecutive adult patients were enrolled in this study, of which 20 (3.2%) developed deep SSI. According to multivariate regression analysis, surgery at academic hospitals (P [ 0.004) and an American Society of Anesthesiologists (ASA) score ‡3 (P [ 0.017) were independent predictors of deep SSI after posterior instrumented fusion surgery for spinal trauma.
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Key words - American Society of Anesthesiologists - Instrumentation - Posterior fusion - Risk factor - Spinal trauma - Surgical site infection Abbreviations and Acronyms ASA: American Society of Anesthesiologists MI: Minimally invasive SSI: Surgical site infection From the 1Department of Orthopaedic Surgery and 2Information Technology Center, Saitama Medical University, Saitama; Departments of Orthopaedic Surgery, 3Musashino Red Cross
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INTRODUCTION
S
urgical site infection (SSI) is a threatening postoperative complication in spinal surgeries because it can result in reoperation (washing and surgical debridement), prolonged hospital stays, and increased expenses. Spinal trauma is a unique pathologic condition considered for spinal surgery, and the number of patients who undergo this surgery is smaller than those undergoing surgery for degenerative spinal diseases. Previously, spinal trauma was reported as an independent risk factor for postoperative SSI in the literature.1,2 The development of spinal instrumentation provided immediate stability for unstable traumatized spine with fractures and/or dislocations and may have facilitated early bed leaving, start of rehabilitation, and decreased incidence of complications associated with prolonged bed rest, such as pressure skin ulcers, deep vein thrombosis,
Hospital, Tokyo, 4Saitama Rehabilitation Center, Saitama, 5Faculty of Medicine, Gunma University, Gunma, 6Yokohama Rosai Hospital, Kanagawa, 7Iwai Orthopaedic Medical Hospital, Tokyo, 8Faculty of Medicine, University of Tokyo, Tokyo and 9Saitama Red Cross Hospital, Saitama; 10Department of Spine and Orthopaedic Surgery, Japanese Red Cross Medical Center, Tokyo; 11Department of Orthopaedic Surgery and Musculoskeletal Oncology, Tokyo Metropolitan Komagome Hospital, Tokyo; and 12Department of Orthopaedic Surgery, Sanraku Hospital, Tokyo, Japan To whom correspondence should be addressed: Satoshi Ogihara, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.10.117 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
pulmonary embolism, and pneumonia.3 On the contrary, several reports described the use of spinal instrumentation as an independent risk factor for SSI in spinal surgeries,4,5 especially in case of posterior surgery.4,5 Spinal trauma and the concurrent use of posterior spinal instrumentation can be suspected to cumulatively increase the risk of SSI after spinal surgery. However, at present, there are only a limited number of reports that have investigated the risk factors for SSI after posterior instrumented fusion surgery for traumatized spine. The aim of this study was to determine the precise independent risk factors in adult patients for deep SSI after posterior instrumented fusion surgery for spinal trauma. In this study, we have retrospectively reviewed prospectively collected multicenter observational research data of 623 registered cases. PATIENTS AND METHODS Study Design and Selection Criteria This observational study was conducted from July 1, 2010, to June 30, 2015, involving 10 hospitals in Japan, with a minimum of 12 months of postoperative follow-up for each of the enrolled cases. This study was approved by the institutional review boards of Saitama Medical University, Musashino Red Cross Hospital, University of Tokyo, Sagamihara National Hospital, Saitama Red Cross Hospital, Japanese Red Cross Medical Center, Tokyo Metropolitan Komagome Hospital, Sanraku Hospital, Yokohama Rosai Hospital, and Iwai Orthopedic Medical Hospital. Given the observational nature of this study, the requirement for written consent from the study subjects was waived by the institutional review boards of the participating hospitals. Information for opt-out was posted on the website of Saitama Medical University. The prospectively collected clinical data from the participating hospitals were anonymized and deidentified prior to the analyses. Detailed preoperative and operative patient characteristics were recorded prospectively using a standardized data collection chart. In this study, spinal trauma was defined as spinal fracture and/or dislocation, and cases with pathologic spinal fracture such as tumoral or infectious spinal abnormalities were excluded. Patients included in this study had undergone conventional posterior open instrumented surgery; however, patients who had undergone minimally invasive (MI) surgery with percutaneous pedicle screws were excluded. Patients <18 years and/or who had undergone single-stage anterior-posterior surgery were also excluded. The SSI definition according to the Centers for Disease Control and Prevention6 was used by the participating hospitals, and wound infection that occurred within 12 months of hardware implantation involving the deep soft tissues was considered as deep SSI.6 Data Collection The prospectively obtained preoperative patient characteristics included age at the time of surgery, sex, height, and weight. Preoperative patient-related risk factors of SSI included smoking, diabetes mellitus, body mass index, American Society of Anesthesiologists (ASA) score,7 and preoperative chronic steroid use. Additionally, data of surgery-related factors including operation duration, intraoperative blood loss, anatomic location of the surgery (cervical, thoracic, and/or lumbosacral), emergency surgery, dural tear, use of intraoperative fluoroscopy, use of a bioclean
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room, prophylactic intravenous administration of cefazolin, intrawound administration of powdered vancomycin, and type (academic or nonacademic) of hospital, considered as possible risk factors for SSI, were collected and analyzed. The microbiological culture results from all patients with deep SSI were recorded and assessed. In patients who underwent open debridement, microbial cultures were analyzed to confirm the development of SSI and to determine the subsequent course of treatment. Statistical Analysis The associations between deep SSI and potential risk factors were analyzed. Fisher exact test and Student t test were used for categorical and continuous variables, respectively. Multivariate analysis was performed to evaluate the risk factors of SSI. The significant variables and the variables that correlated (P < 0.20) with SSI in univariate analysis were entered into a stepwise multiple logistic regression model. Statistical analysis was performed using SPSS Statistics version 24 (IBM Corp., Armonk, New York, USA). P ¼ 0.05 was considered statistically significant. RESULTS From July 2010 to June 2015, a total of 623 consecutive patients (292 women and 331 men; mean age, 63.0 years; age range, 18e97 years) from 10 hospitals in Japan were enrolled for this study. Overall, 20 patients (3.2%) developed postoperative deep SSI. The demographic characteristics of the patients included in this study are given in Table 1. With respect to the demographic characteristics, surgery at academic hospitals and ASA score 3 were significantly associated with SSI (P < 0.05), whereas age 61 years, preoperative chronic steroid use, and dural tear were correlated (P < 0.20) with SSI. These results are similar to those obtained from the univariate logistic regression analysis (Table 2). Table 3 shows the results of the multivariate logistic regression analysis, including the variables that correlated with SSI (P < 0.20) in the univariate logistic regression analysis. The results confirmed that surgeries at academic hospitals (P ¼ 0.004; odds ratio, 4.13; 95% confidence interval, 1.58e10.85) and ASA score 3 (P ¼ 0.017; odds ratio, 3.10; 95% confidence interval, 1.22e7.88) were independent predictors of SSI, whereas advanced age (61 years) tended to correlate with risk of SSI (P ¼ 0.077). Microbial cultures were constantly obtained for testing in the 20 patients who had developed deep SSI, and 80.0% of these patients (16 of 20) had a positive culture with a single organism. Staphylococcus aureus was present in 56.3% of the positive cultures (9 of 16), of which 55.6% (5 of 9) were methicillin-resistant S. aureus. Coagulase-negative staphylococci and Pseudomonas aeruginosa were the next most common organisms, both occurring in 12.5% of the positive cultures (2 of 16) (Table 4). DISCUSSION In this study, we sought to identify the independent risk factors in adult patients susceptible to deep SSI after posterior instrumented fusion surgery for spinal trauma. The number of previous studies on SSI after surgeries for spinal trauma is very limited.8-12 This may be because the number of patients who undergo surgeries for
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
Table 1. Demographic Characteristics of the Surgical Site Infection and NoneSurgical Site Infection Groups SSI Group (n [ 20)
Non-SSI Group (n [ 603)
P Value
67.5 18.0
62.8 20.0
0.292
Age 61 years
17 (85.0)
397 (65.8)
0.055
Men
9 (45.0)
322 (53.4)
0.303
22.3 3.3
22.6 3.8
0.761
ASA score 3
8 (40.0)
115 (19.1)
0.028
Diabetes mellitus
3 (15.0)
73 (12.1)
0.449
Characteristics Age (years)
2
Body mass index (kg/m )
Hemodialysis
1 (5.0)
8 (1.32)
0.256
Smoking
2 (10.0)
58 (9.62)
0.591
Preoperative chronic steroid use
3 (15.0)
36 (5.97)
0.123
3 (15.0)
115 (19.1)
0.457
Anatomic location of the surgery Surgery including cervical spine Surgery including thoracic spine
11 (55.0)
329 (54.6)
0.577
Surgery including lumbosacral spine
15 (75.0)
446 (74.0)
0.577
Dural tear
3 (15.0)
42 (7.0)
0.169
Use of an intraoperative fluoroscopy
5 (25.0)
199 (33.0)
0.313
Use of a bioclean room
5 (25.0)
163 (27.0)
0.537
Emergency surgery
5 (25.0)
168 (27.9)
0.504
Operative time (minutes)
213.3 56.3
216.0 92.0
0.839
Intraoperative bleeding (mL)
409.8 529.6
610.1 721.7
0.219
Prophylactic intravenous administration of CEZ
17 (85.0)
550 (91.2)
0.265
Intrawound application of vancomycin powder
4 (20.0)
143 (23.7)
0.471
Surgery at academic hospitals
7 (35.0)
75 (12.4)
0.010
Values are number of patients (%), mean SD, or as otherwise indicated. SSI, surgical site infection; ASA, American Society of Anesthesiologists; CEZ, cefazolin.
spinal trauma is lower. Dubory et al.,11 in a case series of prospectively collected 518 patients with spinal injuries (including anterior and/or posterior procedures), reported a 4. 8% rate of SSI. Cooper et al.12 reported an infection rate of 4. 0% in a retrospective review of 358 patients who underwent instrumented fixation for spinal trauma (including anterior and/ or posterior procedures). In this study, the registered number of cases from multiple centers was 623; to our knowledge, it is the largest sample size to be prospectively collected for posterior instrumented fusion in spinal trauma. In this study, the incidence of deep SSI was 3.2%, which is considered to be a relatively favorable SSI rate in the case of spinal injury.8-12 It has been reported that superficial SSI is difficult to precisely distinguish from delayed wound healing13; therefore, as an accurate definition of wound infection, only deep SSI was investigated in this study. Accordingly, the infection rate may have been lower because of the exclusion of superficial SSI. In this analysis, surgery at academic hospitals was identified as an independent predictor of development of deep SSI. Although a definitive explanation for the increased risk of SSI at academic hospitals may be difficult to deduce from our data alone, several
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characteristics of academic hospitals are speculated as the cause of this increase. First, the academic hospitals participating in this study were all tertiary care referral institutions, and might have encountered more complex spinal trauma cases than nonacademic hospitals. Second, resident education is inherent to the mission of academic hospitals. Schoenfeld et al.14 reported that resident involvement is correlated with higher risk of SSI after spinal arthrodesis in a retrospective review of the American College of Surgeons' National Surgical Quality Improvement Program database. In contrast, Phan et al.15 found that resident participation in cervical and lumbar spine surgeries did not increase complication rates in their multicenter retrospective cohort. In addition, as a consequence of medical student and resident education at academic hospitals, there is a possibility that the number of people in operating rooms and the frequency of door opening may be increased. There are several reports showing that an increased number of people in the operating room is associated with the incidence of SSI,16-18 and that increased door opening frequency is associated with high air bacterial counts in the operating room.18-20 A precise cause for the difference in the SSI rate between academic and nonacademic hospitals observed in our study could not
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
Table 2. Univariate Logistic Regression Analysis for Deep Surgical Site Infection After Posterior Instrumented Fusion for Spinal Trauma Characteristics
OR (95% CI)
P Value
Age 61 years
2.94 (0.85e10.14)
0.088
Male sex
0.714 (0.292e1.748)
0.461
Body mass index
0.981 (0.870e1.107)
0.760
ASA score 3
2.829 (1.130e7.080)
0.026
Diabetes mellitus
1.281 (0.367e4.479)
0.698
Hemodialysis
3.914 (0.466e32.889)
0.209
Smoking
1.044 (0.236e4.613)
0.955
Preoperative chronic steroid use
2.779 (0.778e9.925)
0.115
Surgery including cervical spine
0.749 (0.216e2.598)
0.649
Surgery including thoracic spine
1.018 (0.416e2.492)
0.969
Surgery including lumbosacral spine
Anatomic location of the surgery
1.056 (0.378e2.953)
0.917
Dural tear
2.357 (0.664e8.367)
0.185
Use of an intraoperative fluoroscopy
0.677 (0.242e1.888)
0.456
Use of a bioclean room
0.900 (0.322e2.515)
0.840
Emergency surgery
0.863 (0.309e2.412)
0.779
Operative time
1.000 (0.995e1.005)
0.896
Intraoperative bleeding
0.999 (0.998e1.000)
0.222
Prophylactic intravenous administration of CEZ
0.546 (0.155e1.924)
0.346
Intrawound application of vancomycin powder
0.804 (0.265e2.444)
0.701
Surgery at academic hospitals
3.791 (1.466e9.803)
0.006
OR, odds ratio; CI, confidence interval; ASA, American Society of Anesthesiologists; CEZ, cefazolin.
be determined; however, the aforementioned factors may correlate with an increased risk of wound infection. An ASA score 3 was also found to be significantly associated with an increased risk of deep SSI in our multivariate analysis. Lonjon et al.10 reported that ASA score was a significant predictor of risk during early (3 months) SSI after surgery for traumatized spine, and there have been several studies that have identified
Table 3. Multivariate Logistic Regression Analysis for Deep Surgical Site Infection After Posterior Instrumented Fusion for Spinal Trauma Characteristic
OR (95% CI)
Age 61 years
P Value 0.077
ASA score 3
3.10 (1.22e7.88)
0.017
Preoperative chronic steroid use
0.131
Dural tear
0.153
Surgery at academic hospitals
4.13 (1.58e10.85)
0.004
OR, odds ratio; CI, confidence interval; ASA, American Society of Anesthesiologists.
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ASA score as being independently associated with the incidence of SSI after elective spinal surgeries.4,5,21 The result of this study is consistent with those of previous studies that have described higher ASA scores as a significant predictor for SSI. ASA score was originally developed to preoperatively assess the overall physical status of the patient.6 ASA score is a reliable index for the evaluation of preoperative general condition, and the ASA classification has been reported to achieve 98% reliability (þ1 class) across different anesthesiologists.22 Spinal trauma is a complex clinical entity; however, ASA score can be a relatively accessible and comprehensive indicator of SSI risk. Multivariate analysis of this study revealed that advanced age (61 years) had the tendency to be associated with be an independent risk factor (P ¼ 0.077), similar to that reported by Dubory et al.11 in their case series. Spinal trauma includes the 2 following categories: vertebral fracture without osteoporosis because of high energy injury such as traffic accident or fall from high places, and osteoporotic vertebral fracture because of low energy injury. In this study, the patients were not distinguished according to these categories. However, elderly patients with a high incidence of SSI in our data may have the clinical characteristic of the latter category of spinal trauma. A single-institutional retrospective study described patients with
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SSI RISK FACTOR IN POSTERIOR FUSION SURGERY
Table 4. Microbiological Characteristics of Surgical Site Infection Organisms
Number of Cases
MRSA
5
Methicillin-sensitive Staphylococcus aureus
4
Pseudomonas aeruginosa
2
Methicillin-resistant CoNS
1
CoNS
1
Enterobacter cloacae
1
Citrobacter koseri
1
Serratia marcescens
1
Unknown
4
MRSA, methicillin-resistant S aureus; CoNS, coagulase-negative staphylococci.
osteoporosis as having an increased SSI risk in lumbar elective surgeries.23 Additionally, patients with osteoporotic vertebral fracture are reported to have a statistically significant higher implant removal rate than patients with degenerative disease with SSI after instrumented fusion,24 and there is a previous report that has described cases with osteoporotic vertebral fracture as at a high risk of death from infectious diseases.25 From these previous reports, an association between osteoporotic vertebral fracture and susceptibility to infections is inferred. Kobayashi et al.26 reported that the need for surgery for osteoporotic vertebral fractures has increased in recent periods; accordingly, the association between osteoporosis vertebral fracture and SSI risk is a noteworthy research topic. To precisely investigate the relationship between advanced age, osteoporotic vertebral fractures, and SSI after fusion surgery for spinal trauma, additional research with a prospective study design and large sample size is needed. This study has several limitations. First, the number of patients who developed SSI was relatively small (n ¼ 20), given that only those patients with deep SSI (excluding superficial SSI) after specific types of procedures (posterior instrumented fusion surgery for spinal trauma) were included. Second, this study did not account
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for several previously studied factors associated with spinal trauma, including the number of operated levels,9-11 preoperative neurologic deficit (American Spinal Injury Association grade),11 polytrauma (injury of other organs),11,12 and timing of surgery after admission.9-11 Additionally, we had not distinguished the patients as 2 categories of vertebral fractures, without osteoporosis because of high energy injury and osteoporotic vertebral fracture because of low energy injury, which might have an effect on clinical features after posterior instrumented fusion. Furthermore, patients who had undergone MI surgery with percutaneous pedicle screws were excluded to maintain a homogenous study population. However, several studies have shown a lower SSI incidence after MI transforaminal interbody fusion using percutaneous pedicle screws than after open transforaminal interbody fusion for degenerative diseases.27,28 MI surgery may reduce iatrogenic tissue injury, intraoperative bleeding, and the exposure of the operative wound to bacteria. The impact of MI fusion with percutaneous pedicle screws for spinal trauma on the incidence of SSI could be a subject of further study. The strengths of this study are the relatively large number of surgical procedures and the prospective multicenter research design that allowed for multivariate logistic regression analysis of the detailed data for the potential risk factors of SSI after spinal surgery. CONCLUSIONS We identified that surgery at academic hospitals and ASA score 3 were significantly and independently associated with the occurrence of deep SSI after posterior instrumented fusion surgery for spinal trauma in adult patients. The complexity of patients and resident involvement in surgeries may be greater at academic hospitals than nonacademic hospitals. ASA score can be a comprehensive and accessible tool for surgeons to preoperatively gauge the potential risk of SSI in patients suffering spinal trauma, a complex clinical entity. The result of this study can provide clinicians with improved risk perception when managing patients undergoing posterior fusion for spinal trauma.
ACKNOWLEDGMENTS The authors thank all the spine surgeons of the participating hospitals who supported the surgeries and data collection.
4. Maragakis LL, Cosgrove SE, Martinez EA, Tucker MG, Cohen DB, Perl TM. Intraoperative fraction of inspired oxygen is a modifiable risk factor for surgical site infection after spinal surgery. Anesthesiology. 2009;110:556-562. 5. Veeravagu A, Patil CG, Lad SP, Boakye M. Risk factors for postoperative spinal wound infections after spinal decompression and fusion surgeries. Spine (Phila Pa 1976). 2009;34:1869-1872. 6. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol. 1999;20:250-278.
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7. Owens WD, Felts JA, Spitznagel EL Jr. ASA physical status classifications: a study of consistency of ratings. Anesthesiology. 1978;49:239-243. 8. Rechtine GR, Bono PL, Cahill D, Bolesta MJ, Chrin AM. Postoperative wound infection after instrumentation of thoracic and lumbar fractures. J Orthop Trauma. 2001;15:566-569. 9. Blam OG, Vaccaro AR, Vanichkachorn JS, et al. Risk factors for surgical site infection in the patient with spinal injury. Spine (Phila Pa 1976). 2003; 28:1475-1480. 10. Lonjon G, Dauzac C, Fourniols E, et al. Early surgical site infections in adult spinal trauma: a prospective, multicentre study of infection rates
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and risk factors. Orthop Traumatol Surg Res. 2012;98: 788-794. 11. Dubory A, Giorgi H, Walter A, et al. Surgical-site infection in spinal injury: incidence and risk factors in a prospective cohort of 518 patients. Eur Spine J. 2015;24:543-554. 12. Cooper K, Glenn CA, Martin M, Stoner J, Li J, Puckett T. Risk factors for surgical site infection after instrumented fixation in spine trauma. J Clin Neurosci. 2016;23:123-127. 13. Kao LS, Ghaferi AA, Ko CY, Dimick JB. Reliability of superficial surgical site infections as a hospital quality measure. J Am Coll Surg. 2011;213:231-235. 14. Schoenfeld AJ, Carey PA, Cleveland AW III, Bader JO, Bono CM. Patient factors, comorbidities, and surgical characteristics that increase mortality and complication risk after spinal arthrodesis: a prognostic study based on 5,887 patients. Spine J. 2013;13:1171-1179. 15. Phan K, Phan P, Stratton A, Kingwell S, Hoda M, Wai E. Impact of resident involvement on cervical and lumbar spine surgery outcomes [e-pub ahead of print]. Spine J https://doi.org/10.1016/j.spinee. 2019.07.006, accessed September 30, 2019. 16. Koutsoumbelis S, Hughes AP, Girardi FP, et al. Risk factors for postoperative infection following posterior lumbar instrumented arthrodesis. J Bone Joint Surg Am. 2011;93:1627-1633. 17. Wathen C, Kshettry VR, Krishnaney A, et al. The association between operating room personnel and turnover with surgical site infection in more than 12 000 neurosurgical cases. Neurosurgery. 2016;79:889-894.
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18. Birgand G, Saliou P, Lucet JC. Influence of staff behavior on infectious risk in operating rooms: what is the evidence? Infect Control Hosp Epidemiol. 2015;36:93-106.
26. Kobayashi K, Ando K, Nishida Y, Ishiguro N, Imagama S. Epidemiological trends in spine surgery over 10 years in a multicenter database. Eur Spine J. 2018;27:1698-1703.
19. Andersson AE, Bergh I, Karlsson J, Eriksson BI, Nilsson K. Traffic flow in the operating room: an explorative and descriptive study on air quality during orthopedic trauma implant surgery. Am J Infect Control. 2012;40:750-755.
27. Parker SL, Adogwa O, Witham TF, Aaronson OS, Cheng J, McGirt MJ. Post-operative infection after minimally invasive versus open transforaminal lumbar interbody fusion (TLIF): literature review and cost analysis. Minim Invasive Neurosurg. 2011;54: 33-37.
20. Scaltriti S, Cencetti S, Rovesti S, Marchesi I, Bargellini A, Borella P. Risk factors for particulate and microbial contamination of air in operating theatres. J Hosp Infect. 2007;66:320-326. 21. Gruskay J, Kepler C, Smith J, Radcliff K, Vaccaro A. Is surgical case order associated with increased infection rate after spine surgery? Spine (Phila Pa 1976). 2012;37:1170-1174. 22. Sankar A, Johnson SR, Beattie WS, Tait G, Wijeysundera DN. Reliability of the American Society of Anesthesiologists physical status scale in clinical practice. Br J Anaesth. 2014;113:424-432.
28. Phan K, Rao PJ, Kam AC, Mobbs RJ. Minimally invasive versus open transforaminal lumbar interbody fusion for treatment of degenerative lumbar disease: systematic review and metaanalysis. Eur Spine J. 2015;4:1017-1030.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
23. Lai Q, Song Q, Guo R, et al. Risk factors for acute surgical site infections after lumbar surgery: a retrospective study. J Orthop Surg Res. 2017;12:116.
Received 2 August 2019; accepted 19 October 2019
24. Ishii M, Iwasaki M, Ohwada T, et al. Postoperative deep surgical-site infection after instrumented spinal surgery: a multicenter study. Global Spine J. 2013;3:95-102.
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25. Chen YC, Lin WC. Risk of long-term infectionrelated death in clinical osteoporotic vertebral fractures: a hospital-based analysis. PLoS One. 2017;12:e0182614.
Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.10.117
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.10.117