British Journal of Neurosurgery, April 2014; 28(2): 270–275 © 2014 The Neurosurgical Foundation ISSN: 0268-8697 print / ISSN 1360-046X online DOI: 10.3109/02688697.2013.835376
ORIGINAL ARTICLE
Surgical site infections in standard neurosurgery procedures– a study of incidence, impact and potential risk factors Sami Abu Hamdeh1, Birgitta Lytsy2 & Elisabeth Ronne-Engström1 1Department of Neuroscience, Section of Neurosurgery, Uppsala University, Uppsala Sweden, and 2Department of Medical
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Sciences, Section of Clinical Microbiology and Infectious Diseases, Uppsala University, Uppsala, Sweden
Introduction
Abstract Objectives. Surgical site infections (SSIs) may be devastating for the patient and they carry high economic costs. Studies of SSI after neurosurgery report an incidence of 1–11%. However, patient material, follow-up time and definition of SSI have varied. In the present study we prospectively recorded the prevalence of SSI 3 months after standard intracranial neurosurgical procedures. The incidence, impact and risk factors of SSI were analysed. Methods. We included patients admitted during 2010 to our unit for postoperative care after standard neurosurgical procedures. SSI was defined as evident with positive cultures from surgical samples or CSF, and/or purulent discharge during reoperation. Follow-up was done after 3 and 12 months and statistics was obtained after 3 months. The predictive values on the outcome of demographic and clinical factors describing the surgical procedure were evaluated using linear regression. Results. A total of 448 patients were included in the study and underwent a total of 466 procedures. Within 3 and 12 months, 33 and 88 patients, respectively, had died. Of the surviving patients, 20 (4.3% of procedures) developed infections within 3 months and another 3 (4.9% of procedures) within 12 months. Risk factors for SSI were meningioma, longer operation time, craniotomy, dural substitute, and staples in wound closure. Patients with SSI had significantly longer hospital stay. Multivariate analysis showed that factors found significant in univariate analysis frequently occur together. Discussion. We studied the prevalence of SSI after 3 and 12 months in a prospective 1-year material with standard neurosurgical procedures and found it to be 4.3% and 4.9%, respectively. The analysis of the results showed that a combination of parameters indicating a longer and more complicated procedure predicted the development of SSI. Our conclusion is that the prevention of SSI has to be done at many levels, especially with patients undergoing long surgical procedures.
Postoperative infections after neurosurgical procedures carry a high morbidity rate and not uncommonly have a life-threatening potential. SSIs also carry high economic and environmental costs including prolonged hospitalisation and the development of antibioticresistant bacteria. Surgical site infections (SSIs) following neurosurgical operations usually require long-term antibiotic treatment and frequent reoperation, for example bone flap removal due to osteomyelitis after craniotomy or the evacuation of subdural empyema or brain abscess. In a recent study O´Keeffe and colleagues estimated the cost for SSIs after craniotomy to be over £9000 for each case of infection.1 Studies of postoperative infections after neurosurgery have typically reported an incidence of about 5% with a range of 1–11%.1–6 Comparisons between earlier studies are difficult, since patient material and definition of infections have varied. Also, the time to follow-up is in many cases unclear, especially in the retrospective reports. Higher rates of infection are seen in the presence of risk factors such as repeated surgery, operations lasting longer than 4 h, CSF leakage, operations involving nasal sinuses, and emergency operations. The most frequently found offending organisms in SSIs after neurosurgical procedures from previous series are Staphylococcus Aureus2–4 indicating contamination from the skin. Coagulase-Negative Staphylococci (CNS) and Propionebacterium species are also common findings. Preoperative antibiotic prophylactics targeting these microbes can lower the SSI incidence5–7 and is standard treatment at neurosurgical units. In the present prospective study, we measured the incidence of SSI at 3 and 12 months following discharge after defined standard neurosurgical procedures. We have also characterised the primary risk factors for patients in our clinic developing SSI.
Keywords: craniotomy; neurosurgery; prospective; risk factors for infection; surgical site infections
Correspondence: Sami Abu Hamdeh, Department of Neuroscience, Uppsala University, Section of Neurosurgery, Akademiska Sjukhuset, Uppsala 751 85, Sweden. E-mail: [email protected] Received for publication 6 February 2013; accepted 11 August 2013
270
SSI in standard neurosurgery procedures
Material and methods
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Patients We included patients admitted to our intermediate-care post-operative ward (NIMA) during 2010 after having been operated for intracranial tumours, chronic subdural haematomas or reconstructive cranioplasty. The surgical procedures for the tumours included removal or resection through craniotomies and craniectomies, and biopsies through burr holes. Petrosectomies, transnasal approaches and spine cases were excluded as well as patients treated pre- or postoperatively in the neurointensive care unit. The reason for the exclusion of these patients was to facilitate the creation of a database for continuous supervision of SSI rates in our department, where we wanted a homogenous group and a foreseeable number of patients. A total of 448 patients admitted to NIMA during 2010 met our criteria and were included in the study. Of the included patients 268 (54.9%) were males. Median age was 64 years (range 6–92). Fourteen patients underwent two or more procedures. The majority of operations in the present study were performed for intracranial tumours (Table I) (54.5% of procedures, with high-grade glioma being the most common (21.7%)) followed by burr-hole craniectomy for chronic subdural haematoma (29.4%). Of all procedures 37.6% were performed in an emergency setting, and 62.4% were elective. Mean operating time was 3 h 23 min. Virtually all patients received antibiotic prophylactics before surgery (99.1%). Cloxacillin was the antibiotic of choice in most cases (92.1%) followed by Clindamycin (5.4%), used in the presence or suspicion of penicillin allergy. Forty patients (8.9%) had a record of diabetes and 220 were on steroid treatment before undergoing surgery (49.1%). After 3-month follow-up 33 patients had deceased (7.4%), and after 12 months a total of 88 patients had died (19.6%).
Data collection Data were collected using the electronic patient journal system. We collected demographic data as gender, age and diagnosis, as well as factors suspected to influence the risk for wound infections. This included the occurrence of diabetes, steroid treatment, antibiotic prophylactics, type of antibiotics, blood replacement therapy, type of surgical procedure, duration of surgery, used operating theatre, number of people in the operating room during surgery, inserted surgical implants, use of wound drainage, technique for skin closure and hair removal. Table I. This table shows the number of patients with each diagnosis and those that developed a SSI. No. of Infected Percent of Diagnosis operations patients infections (%) SDH Glioma Meningioma Cranioplasty Metastasis Chiari Colloid cyst Vascular Other tumours Miscellaneous
140 120 83 38 25 11 6 9 30 4
3 3 10 3 1 1 1 1 0 0
2.1 2.5 12 7.9 4 9 16.7 11.1 0 0
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Surgical site infection in the present study was defined as evident with positive cultures from surgical samples or CSF, and/or evidence of purulent discharge from wound or deep intracranial infection during reoperation. Incidence of SSI was controlled after 3 and 12 months, respectively, in accordance with Centers of Disease Control and Prevention (CDC) criteria,8 since neurosurgical procedures usually imply insertion of surgical implants. The follow-up was done by consulting the electronic medical records at 3 and 12 months. This strategy was based on the experience that referring physicians contact our clinic immediately when problems are encountered with operated patients, and all communication is then done through the electronic medical records, making sure no information is lost. Since our department is the only unit in our region with neurosurgical expertise, we are always consulted when there is a suspected complication after surgery. Patients with clinical or radiological suspicion of SSI after a neurosurgical procedure are therefore readmitted for further investigation and surgery if needed.
Statistics Statistica 10.0 (Stat Soft, Inc. Tulsa, OK) was used for descriptive and analytical statistics. Categorical variables were compared using Fisher’s exact test and continuous variables using t-test. We included a fairly large number of variables in the analysis. This created a high dimensionality making the material difficult to overview. Therefore we used principal components analysis with Non-linear Iterative Partial Least Squares (NIPALS) to illustrate our material. NIPALS is a mathematical procedure that aims to represent a set of (possibly correlated) multivariate variables with the aid of a smaller number of uncorrelated variables known as principal components. Using NIPALS we defined two principal components: p1 and p2 (Fig. 1). The figure shows the influence of each variable on p1 and p2, respectively. This is called the variables loading factors and is plotted on the x-axis for p1 and on the y-axis for p2. Figure 1 demonstrates that some variables are clustered (placed close to each other). Clustered variables influence the model in similar ways, which also indicates they are correlated. We analysed the risk factors further using a generalised linear model with a multinomial ordinal response and a logistic link function. The best subset of predictive variables for SSI was selected using Aikake’s Information Criterion.9 A p value ⬍ 0.05 was considered statistically significant.
Ethics The Uppsala University Regional Ethical Review Board for clinical research granted permission for the study.
Results Prevalence of infections Twenty cases were complicated by surgical site infection after 3 months of follow-up and after 12 months of follow-up, three more cases of surgical site infection were identified. Out of the 23 cases complicated by SSI, three patients eventually died within the 12 months of follow-up. Incidence of SSI was 4.3% of all procedures (4.5% of patients) after
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S. Abu Hamdeh et al.
Fig. 1. In this figure we used Principal components analysis with NIPALS in order to illustrate our material. Some variables such as dural substitute, diagnosis of meningioma and skin closure are clustered. This means that they influence the model in similar ways, which also indicates that they are correlated.
3 months and 4.9% of all procedures (5.1% of patients) after 12 months follow-up. In the infected group 12 patients were men (52.2%) and 11 women (47.8%). Median age was 62 years (range 18–86). A total of 26 operations were performed in the infected group (17 elective and 9 emergency procedures). Three patients had undergone ⱖ 2 procedures: two patients for bilateral chronic subdural haematoma and one patient for a postoperative bleeding after the initial evacuation of a subdural haematoma. The most common surgical site infection was bone flap osteomyelitis that was seen alone in 6 cases (26.1% of infected patients) and in conjunction with a brain abscess in 5 additional cases (21.7%). Bone flap osteomyelitis and subdural empyema were seen together in 2 cases (8.7%). One patient had bone flap osteomyelitis, brain abscess and evidence of meningitis with positive cultures in CSF, whereas meningitis alone affected two patients (8.7%). In three patients, infection after cranial reconstruction was seen (13%), seated on the synthetic bone substitute in one case and on cryo-preserved bone flap in two cases. The remaining four cases (17.4%) had only an infection affecting the skin. Mean operation time in the infected group was 4 h 12 min. Diagnoses affected are indicated in Table I. Three of the 23 patients with SSI presented with fever ⬎ 38.5° when readmitted to hospital. One patient presented with seizures whereas a total of five patients presented with confused mental state. Leucocytosis was seen in 9 patients (39%) and a rise in C-reactive protein in 14 patients (61%). Radiological evidence of intracranial infection such as epidural, subdural or intracranial fluid accumulation with irregular contrast enhancement and bone resorption on contrastenhanced computed tomography, or restricted diffusion on magnetic resonance tomography in cases of suspected
intracerebral abscess was seen in 13 patients (57%) as shown in Fig. 2a and b. The most common offending organism was CNS (34.8%) followed by Propionebacterium species (26.1%) and Staphylococcus aureus (21.7%) as seen in Table II. Seventeen patients
Fig. 2. (a) Contrast-enhanced CT of patients operated for parietotemporal meningioma. Images demonstrate fluid accumulation in postoperative cavity and extradurally with contrast-enhancing capsule, as well as underlying brain oedema. (b) Contrast-enhanced CT images of patients operated with cranioplasty of own bone after hemicraniectomy for malignant middle cerebral artery infarction. Images demonstrate large epidural fluid accumulation with irregular contrast-enhancing capsule as well as evidence of osteomyelitis.
SSI in standard neurosurgery procedures Table II. This table lists the bacteria found in cultures from the infected surgical wounds. No. of Bacteria patients Percent (%)
Table III. This table lists the results from the univariate analysis of risk factors from SSI. Mean operations Mean infected p value
CNS Propionebacterium Staphylococcus Aureus Enterobacter aerogenes CNS ⫹ Propionebacterium CNS ⫹ Propionebacterium ⫹ enterococcus No positive culture
Age Theatre staff Length of stay Operation time
8 6 5 1 1 1 1
34.8 26.1 21.7 4.3 4.3 4.3 4.3
Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI.
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needed one reoperation after readmission for SSI, and six patients needed more than one reoperation. In 13 patients additional surgery was necessary for cranial reconstruction at a later stage after controlling infection.
62 years 8.4 persons 9 days 3 h 23 min
Due to the loss of 88 patients who died within 12 months, statistical analysis was performed after 3 months. Tables III and IV list variables that were considered as possible risk factors for the development of SSI. Individual factors that were found to be statistically significant (p ⬍ 0.05) were prolonged length of hospital stay, prolonged operation time, craniotomy as the method of surgery, use of dural substitute, and use of staples for skin closure. Among the diagnoses, operated meningioma was found as a statistically significant risk factor for the development of SSI (Table V). No significant difference was found between operating theatres. Variables found statistically significant in univariate analysis were included in multivariate logistic regression. A significant correlation (Spearman’s R) was found between length of operation time and length of hospital stay. Therefore length of stay was not included in analysis. Results of multivariate modelling are seen in Table VI. The best subsets of variables predicting the development of SSI included dural
Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI.
substitute, operation time, method for skin closure, and surgical method. To illustrate how these are correlated we also did a principal component analysis (see methods) (Fig. 1). This figure shows that staples for skin closure, long surgery time, dural substitute and meningioma are clustered, indicating that they frequently occur together.
Prevalence of surgical site infection The background for our study was that we wanted to define a patient group that could be used for future control of the quality of our routines pertaining to surgical procedures. Therefore we included all patients operated for intracranial tumours, chronic subdural haematomas and reconstructive cranioplasty who were admitted to our post-operative ward. Contrary to other published materials we set a fixed follow-up time of 3 and 12 months. According to CDC as well as Swedish standards, surgery with implants like bone flap fixating material has to be followed up for 12 months in order to rule out infection.10 The prevalence in our study was 4.3% of all procedures after 3 months where 20 of the infections occurred. Another three infections occurred between 3 and 12 months, making the prevalence 4.9% of all procedures. During this time, however, 88 patients from the original group died, making the 12-month prevalence difficult to interpret. Due to the health care organisation we believe that we were
Table IV. This table lists the results from the univariate analysis of risk factors from SSI. No. of operations No. infected % Infected
Admission Time of surgery Diabetes Steroids Blood transfusion Hair removal Wound drainage Method of surgery Dural substitute Wound closure
n.s n.s ⬍ 0.02 ⬍ 0.03
Discussion
Risk factors for infections
Gender
61 years 9.3 persons 13 days 4 h 12 min
258 Men 208 Women 175 Acute 291 Elective 368 Work hours 124 On call 39 Yes 427 No 222 Yes 244 No 54 Yes 411 No 239 Complete 226 Partial 378 Yes 88 No 192 Craniectomy 274 Craniotomy/ 36 Yes 430 No 158 Staples 307 Sutures
15 Men 11 Women 9 Acute 17 Elective 21 Work hours 5 On call 2 Yes 24 No 13 Yes 13 No 4 Yes 22 No 17 Complete 9 Partial 19 Yes 7 No 6 Craniectomy 20 Craniotomy 8 Yes 18 No 14 Staples 12 Sutures
3.2% 2.4% 1.9% 3.6% 4.5% 1.1% 0.4% 5.2% 2.8% 2.8% 0.9% 4.7% 3.7% 1.9% 4.1% 1.5% 1.3% 4.3% 1.7% 3.9% 3.0% 2.6%
p value n.s n.s n.s n.s n.s n.s n.s n.s ⬍ 0.04 ⬍ 0.0003 ⬍ 0.03
Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI, n.s. Not significant.
274 S. Abu Hamdeh et al. Table V. This table lists the results from the univariate analysis of risk factors from SSI. No. of operations No. infected % Infected p value Glioma/Mets Meningioma SDH Cranioplasty Miscellaneous
127 Operations 82 Operations 129 Operations 38 Operations 57 Operations
4 Infections 10 Infections 6 Infections 3 Infections 3 Infections
0.9% 2.3% 1.4% 0.7% 0.7%
n.s ⬍ 0.02 n.s n.s n.s
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Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI.
consulted regarding all cases of SSI, but it cannot be ruled out that there were some more, for example with terminal brain tumours. Our results are in line with other studies that demonstrate an SSI prevalence of 1–11%.1,2,4,10–12 However, most of other published studies describe almost the entire surgical material in one department. Therefore, these other materials are very heterogeneous regarding diagnoses, risk factors and treatments other than surgery. Another large problem is that the follow-up times have varied, ranging from 2 weeks4 to mean 13.5 months.11 Three of the larger studies did not provide any information at all about the follow-up time.2,10,13 It is the latter two of these that reported the lowest incidences of infection. It is therefore difficult to make accurate comparisons between our results and earlier studies. In our material bone flap osteomyelitis was the most common finding, alone or in combination with abscess, subdural empyema or superficial infection. A total of 20/22 patients had cutaneous pathogens as the offending organisms, one of them in combination with Enterococcus fecalis. One had Enterobacter aerogenes only. In another obviously purulent case we had no positive cultures.
Risk factors We found in the univariate analysis that the surgical method craniotomy, use of dural substitute, diagnosis of meningioma, and wound closure with staples were significantly more common in cases with SSI. Longer duration of the surgical procedure was also associated with increased risk for infections. The findings regarding long surgery and implants are consistent with other studies.
Parameters such as dural substitute, diagnosis of meningiomas, and longer surgery frequently occur together as illustrated with principal components analysis (Fig. 1). It is therefore difficult to point out single factor as responsible. We think instead that these parameters indicate a more complicated surgical situation, which increases the possibilities for the wound to be exposed to bacteria. It seems that this situation is more common in surgery of meningiomas in our material. On the other hand, the fact that these variables were selected into the same multivariate model (Table VI) indicates that each has some independent predictive power. Common sense precautions such as reducing door openings, using as non-traumatic techniques as possible and monitoring air quality should be applied, especially during lengthy procedures. Other factors such as hair removal, wound drain, age, gender, number of people in the operating room, diabetes, steroids and blood transfusion were not related to increased risk for SSI. We found that more than 99% of patients received prophylactic antibiotics in accordance with the department’s protocol. The importance of prophylactic antibiotics has been demonstrated earlier.5,11,13 As described in detail by the Surgical Infection Prevention Project it is not enough simply to administer antibiotics; it is necessary to match the type of antibiotic used with the most common cutaneous pathogens, and to optimise timing, redosing and discontinuation.
Impact of SSI Patients who developed SSI required readmission, reoperation and antibiotic therapy in order to control the infection. In 13 cases further surgery was necessary for cranial reconstruction after the infection had been controlled. One patient developed hemiparesis after presenting with subdural empyema. This illustrates the high socio-economic cost of SSI, which was estimated in earlier studies, as well as the patient suffering SSI causes.5
Conclusion In this study we measured the 3- and 12-month prevalence of SSI after 466 craniotomies and craniectomies
Table VI. This table shows the best subsets of variables predicting SSI. Dural substitute stands out as important, in combination with surgery duration and method for skin closure. Degree of Variable 1 Variable 2 Variable 3 Variable 4 freedom AIC L.Ratio Chi2 p value Dural substitute Dural substitute Dural substitute Dural substitute Method of surgery Method of surgery Method of surgery Method of surgery Operation time Skin closure Skin closure Method of surgery Skin closure Skin closure Method of surgery
Operation time Skin closure Skin closure Dural substitute Dural substitute Dural substitute Dural substitute
Operation time Method of surgery Skin closure Skin closure
Operation time Operation time Method of surgery Method of surgery
Operation time
Operation time
1 2 2 3 2 3 3 4 1 2 1 2 3 2 1
170.0146 170.2706 170.3912 171.0302 171.7102 172.2108 172.3870 172.9546 173.8141 173.9941 174.8053 175.6570 175.9274 176.8035 176.8366
7.64083 9.38483 9.26417 10.62518 7.94517 9.44461 9.26838 10.70081 3.84134 5.66132 2.85007 3.99835 5.72802 2.85187 0.81881
⬍ 0.006 ⬍ 0.01 ⬍ 0.01 ⬍ 0.02 ⬍ 0.02 ⬍ 0.03 ⬍ 0.03 ⬍ 0.04 n.s n.s n.s n.s n.s n.s n.s
SSI in standard neurosurgery procedures
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that received postoperative care in the intermediate ward. The SSI prevalence was 4.3% after 3 months. A total of 88 patients died between 3 and 12 months. Only three additional patients (0.8%) developed an SSI during the same 9-month period. Longer surgery time, meningioma, use of dural substitute and skin closure with staples all were significantly associated with the development of SSI after 3 months. Factors contributing to the risk of SSI indicate a more complex surgical situation. These cases require especially stringent safeguards against infection, as well as careful monitoring following surgery in order to detect SSI at an early stage.
Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. O’Keeffe AB, Lawrence T, Bojanic S. Oxford craniotomy infections database: A cost analysis of craniotomy infection. Br J Neurosurg 2012;26:265–9. 2. McClelland S III, Hall WA . Postoperative central nervous system infection: incidence and associated factors in 2111 neurosurgical procedures. Clin Infect Dis 2007;45:55–9.
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3. Dashti SR, Baharvahdat H, Spetzler RF, et al. Operative intracranial infection following craniotomy. Neurosurg Focus 2008;24: E10. 4. Erman T, Demirhindi H, Gocer AI, et al. Risk factors for surgical site infections in neurosurgery patients with antibiotic prophylaxis. Surg Neurol 2005;63:107–112; discussion 112–103. 5. Barker FG II. Efficacy of prophylactic antibiotics for craniotomy: a meta-analysis. Neurosurgery 1994;35:484–90; discussion 491–82. 6. Barker FG II. Efficacy of prophylactic antibiotics against meningitis after craniotomy: a meta-analysis. Neurosurgery 2007;60:887–94; discussion 887–94. 7. Raggueneau JL, Cophignon J, Kind A , et al. [analysis of infectious sequelae of 1000 neurosurgical operations. Effects of prophylactic antibiotherapy]. Neuro-Chirurgie 1983;29:229–33. 8. Horan TC, Andrus M, Dudeck MA . Cdc/nhsn surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309–32. 9. Akaike. A new look at the statistical model identification. IEEE Trans Automat Control 1974;19:716–23. 10. Valentini LG, Casali C, Chatenoud L, et al. Surgical site infections after elective neurosurgery: a survey of 1747 patients. Neurosurgery 2008;62:88–95; discussion 95–86. 11. Blomstedt GC. Infections in neurosurgery: a retrospective study of 1143 patients and 1517 operations. Acta Neurochir 1985;78:81–90. 12. Korinek AM. Risk factors for neurosurgical site infections after craniotomy: a prospective multicenter study of 2944 patients. The french study group of neurosurgical infections, the sehp, and the c-clin paris-nord. Service epidemiologie hygiene et prevention. Neurosurgery 1997;41:1073–9; discussion 1079–81. 13. Korinek AM, Golmard JL, Elcheick A , et al. Risk factors for neurosurgical site infections after craniotomy: a critical reappraisal of antibiotic prophylaxis on 4,578 patients. Br J Neurosurg 2005;19: 155–62.
ORIGINAL ARTICLE
Surgical site infections in standard neurosurgery procedures– a study of incidence, impact and potential risk factors Sami Abu Hamdeh1, Birgitta Lytsy2 & Elisabeth Ronne-Engström1 1Department of Neuroscience, Section of Neurosurgery, Uppsala University, Uppsala Sweden, and 2Department of Medical
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Sciences, Section of Clinical Microbiology and Infectious Diseases, Uppsala University, Uppsala, Sweden
Introduction
Abstract Objectives. Surgical site infections (SSIs) may be devastating for the patient and they carry high economic costs. Studies of SSI after neurosurgery report an incidence of 1–11%. However, patient material, follow-up time and definition of SSI have varied. In the present study we prospectively recorded the prevalence of SSI 3 months after standard intracranial neurosurgical procedures. The incidence, impact and risk factors of SSI were analysed. Methods. We included patients admitted during 2010 to our unit for postoperative care after standard neurosurgical procedures. SSI was defined as evident with positive cultures from surgical samples or CSF, and/or purulent discharge during reoperation. Follow-up was done after 3 and 12 months and statistics was obtained after 3 months. The predictive values on the outcome of demographic and clinical factors describing the surgical procedure were evaluated using linear regression. Results. A total of 448 patients were included in the study and underwent a total of 466 procedures. Within 3 and 12 months, 33 and 88 patients, respectively, had died. Of the surviving patients, 20 (4.3% of procedures) developed infections within 3 months and another 3 (4.9% of procedures) within 12 months. Risk factors for SSI were meningioma, longer operation time, craniotomy, dural substitute, and staples in wound closure. Patients with SSI had significantly longer hospital stay. Multivariate analysis showed that factors found significant in univariate analysis frequently occur together. Discussion. We studied the prevalence of SSI after 3 and 12 months in a prospective 1-year material with standard neurosurgical procedures and found it to be 4.3% and 4.9%, respectively. The analysis of the results showed that a combination of parameters indicating a longer and more complicated procedure predicted the development of SSI. Our conclusion is that the prevention of SSI has to be done at many levels, especially with patients undergoing long surgical procedures.
Postoperative infections after neurosurgical procedures carry a high morbidity rate and not uncommonly have a life-threatening potential. SSIs also carry high economic and environmental costs including prolonged hospitalisation and the development of antibioticresistant bacteria. Surgical site infections (SSIs) following neurosurgical operations usually require long-term antibiotic treatment and frequent reoperation, for example bone flap removal due to osteomyelitis after craniotomy or the evacuation of subdural empyema or brain abscess. In a recent study O´Keeffe and colleagues estimated the cost for SSIs after craniotomy to be over £9000 for each case of infection.1 Studies of postoperative infections after neurosurgery have typically reported an incidence of about 5% with a range of 1–11%.1–6 Comparisons between earlier studies are difficult, since patient material and definition of infections have varied. Also, the time to follow-up is in many cases unclear, especially in the retrospective reports. Higher rates of infection are seen in the presence of risk factors such as repeated surgery, operations lasting longer than 4 h, CSF leakage, operations involving nasal sinuses, and emergency operations. The most frequently found offending organisms in SSIs after neurosurgical procedures from previous series are Staphylococcus Aureus2–4 indicating contamination from the skin. Coagulase-Negative Staphylococci (CNS) and Propionebacterium species are also common findings. Preoperative antibiotic prophylactics targeting these microbes can lower the SSI incidence5–7 and is standard treatment at neurosurgical units. In the present prospective study, we measured the incidence of SSI at 3 and 12 months following discharge after defined standard neurosurgical procedures. We have also characterised the primary risk factors for patients in our clinic developing SSI.
Keywords: craniotomy; neurosurgery; prospective; risk factors for infection; surgical site infections
Correspondence: Sami Abu Hamdeh, Department of Neuroscience, Uppsala University, Section of Neurosurgery, Akademiska Sjukhuset, Uppsala 751 85, Sweden. E-mail: [email protected] Received for publication 6 February 2013; accepted 11 August 2013
270
SSI in standard neurosurgery procedures
Material and methods
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Patients We included patients admitted to our intermediate-care post-operative ward (NIMA) during 2010 after having been operated for intracranial tumours, chronic subdural haematomas or reconstructive cranioplasty. The surgical procedures for the tumours included removal or resection through craniotomies and craniectomies, and biopsies through burr holes. Petrosectomies, transnasal approaches and spine cases were excluded as well as patients treated pre- or postoperatively in the neurointensive care unit. The reason for the exclusion of these patients was to facilitate the creation of a database for continuous supervision of SSI rates in our department, where we wanted a homogenous group and a foreseeable number of patients. A total of 448 patients admitted to NIMA during 2010 met our criteria and were included in the study. Of the included patients 268 (54.9%) were males. Median age was 64 years (range 6–92). Fourteen patients underwent two or more procedures. The majority of operations in the present study were performed for intracranial tumours (Table I) (54.5% of procedures, with high-grade glioma being the most common (21.7%)) followed by burr-hole craniectomy for chronic subdural haematoma (29.4%). Of all procedures 37.6% were performed in an emergency setting, and 62.4% were elective. Mean operating time was 3 h 23 min. Virtually all patients received antibiotic prophylactics before surgery (99.1%). Cloxacillin was the antibiotic of choice in most cases (92.1%) followed by Clindamycin (5.4%), used in the presence or suspicion of penicillin allergy. Forty patients (8.9%) had a record of diabetes and 220 were on steroid treatment before undergoing surgery (49.1%). After 3-month follow-up 33 patients had deceased (7.4%), and after 12 months a total of 88 patients had died (19.6%).
Data collection Data were collected using the electronic patient journal system. We collected demographic data as gender, age and diagnosis, as well as factors suspected to influence the risk for wound infections. This included the occurrence of diabetes, steroid treatment, antibiotic prophylactics, type of antibiotics, blood replacement therapy, type of surgical procedure, duration of surgery, used operating theatre, number of people in the operating room during surgery, inserted surgical implants, use of wound drainage, technique for skin closure and hair removal. Table I. This table shows the number of patients with each diagnosis and those that developed a SSI. No. of Infected Percent of Diagnosis operations patients infections (%) SDH Glioma Meningioma Cranioplasty Metastasis Chiari Colloid cyst Vascular Other tumours Miscellaneous
140 120 83 38 25 11 6 9 30 4
3 3 10 3 1 1 1 1 0 0
2.1 2.5 12 7.9 4 9 16.7 11.1 0 0
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Surgical site infection in the present study was defined as evident with positive cultures from surgical samples or CSF, and/or evidence of purulent discharge from wound or deep intracranial infection during reoperation. Incidence of SSI was controlled after 3 and 12 months, respectively, in accordance with Centers of Disease Control and Prevention (CDC) criteria,8 since neurosurgical procedures usually imply insertion of surgical implants. The follow-up was done by consulting the electronic medical records at 3 and 12 months. This strategy was based on the experience that referring physicians contact our clinic immediately when problems are encountered with operated patients, and all communication is then done through the electronic medical records, making sure no information is lost. Since our department is the only unit in our region with neurosurgical expertise, we are always consulted when there is a suspected complication after surgery. Patients with clinical or radiological suspicion of SSI after a neurosurgical procedure are therefore readmitted for further investigation and surgery if needed.
Statistics Statistica 10.0 (Stat Soft, Inc. Tulsa, OK) was used for descriptive and analytical statistics. Categorical variables were compared using Fisher’s exact test and continuous variables using t-test. We included a fairly large number of variables in the analysis. This created a high dimensionality making the material difficult to overview. Therefore we used principal components analysis with Non-linear Iterative Partial Least Squares (NIPALS) to illustrate our material. NIPALS is a mathematical procedure that aims to represent a set of (possibly correlated) multivariate variables with the aid of a smaller number of uncorrelated variables known as principal components. Using NIPALS we defined two principal components: p1 and p2 (Fig. 1). The figure shows the influence of each variable on p1 and p2, respectively. This is called the variables loading factors and is plotted on the x-axis for p1 and on the y-axis for p2. Figure 1 demonstrates that some variables are clustered (placed close to each other). Clustered variables influence the model in similar ways, which also indicates they are correlated. We analysed the risk factors further using a generalised linear model with a multinomial ordinal response and a logistic link function. The best subset of predictive variables for SSI was selected using Aikake’s Information Criterion.9 A p value ⬍ 0.05 was considered statistically significant.
Ethics The Uppsala University Regional Ethical Review Board for clinical research granted permission for the study.
Results Prevalence of infections Twenty cases were complicated by surgical site infection after 3 months of follow-up and after 12 months of follow-up, three more cases of surgical site infection were identified. Out of the 23 cases complicated by SSI, three patients eventually died within the 12 months of follow-up. Incidence of SSI was 4.3% of all procedures (4.5% of patients) after
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S. Abu Hamdeh et al.
Fig. 1. In this figure we used Principal components analysis with NIPALS in order to illustrate our material. Some variables such as dural substitute, diagnosis of meningioma and skin closure are clustered. This means that they influence the model in similar ways, which also indicates that they are correlated.
3 months and 4.9% of all procedures (5.1% of patients) after 12 months follow-up. In the infected group 12 patients were men (52.2%) and 11 women (47.8%). Median age was 62 years (range 18–86). A total of 26 operations were performed in the infected group (17 elective and 9 emergency procedures). Three patients had undergone ⱖ 2 procedures: two patients for bilateral chronic subdural haematoma and one patient for a postoperative bleeding after the initial evacuation of a subdural haematoma. The most common surgical site infection was bone flap osteomyelitis that was seen alone in 6 cases (26.1% of infected patients) and in conjunction with a brain abscess in 5 additional cases (21.7%). Bone flap osteomyelitis and subdural empyema were seen together in 2 cases (8.7%). One patient had bone flap osteomyelitis, brain abscess and evidence of meningitis with positive cultures in CSF, whereas meningitis alone affected two patients (8.7%). In three patients, infection after cranial reconstruction was seen (13%), seated on the synthetic bone substitute in one case and on cryo-preserved bone flap in two cases. The remaining four cases (17.4%) had only an infection affecting the skin. Mean operation time in the infected group was 4 h 12 min. Diagnoses affected are indicated in Table I. Three of the 23 patients with SSI presented with fever ⬎ 38.5° when readmitted to hospital. One patient presented with seizures whereas a total of five patients presented with confused mental state. Leucocytosis was seen in 9 patients (39%) and a rise in C-reactive protein in 14 patients (61%). Radiological evidence of intracranial infection such as epidural, subdural or intracranial fluid accumulation with irregular contrast enhancement and bone resorption on contrastenhanced computed tomography, or restricted diffusion on magnetic resonance tomography in cases of suspected
intracerebral abscess was seen in 13 patients (57%) as shown in Fig. 2a and b. The most common offending organism was CNS (34.8%) followed by Propionebacterium species (26.1%) and Staphylococcus aureus (21.7%) as seen in Table II. Seventeen patients
Fig. 2. (a) Contrast-enhanced CT of patients operated for parietotemporal meningioma. Images demonstrate fluid accumulation in postoperative cavity and extradurally with contrast-enhancing capsule, as well as underlying brain oedema. (b) Contrast-enhanced CT images of patients operated with cranioplasty of own bone after hemicraniectomy for malignant middle cerebral artery infarction. Images demonstrate large epidural fluid accumulation with irregular contrast-enhancing capsule as well as evidence of osteomyelitis.
SSI in standard neurosurgery procedures Table II. This table lists the bacteria found in cultures from the infected surgical wounds. No. of Bacteria patients Percent (%)
Table III. This table lists the results from the univariate analysis of risk factors from SSI. Mean operations Mean infected p value
CNS Propionebacterium Staphylococcus Aureus Enterobacter aerogenes CNS ⫹ Propionebacterium CNS ⫹ Propionebacterium ⫹ enterococcus No positive culture
Age Theatre staff Length of stay Operation time
8 6 5 1 1 1 1
34.8 26.1 21.7 4.3 4.3 4.3 4.3
Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI.
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needed one reoperation after readmission for SSI, and six patients needed more than one reoperation. In 13 patients additional surgery was necessary for cranial reconstruction at a later stage after controlling infection.
62 years 8.4 persons 9 days 3 h 23 min
Due to the loss of 88 patients who died within 12 months, statistical analysis was performed after 3 months. Tables III and IV list variables that were considered as possible risk factors for the development of SSI. Individual factors that were found to be statistically significant (p ⬍ 0.05) were prolonged length of hospital stay, prolonged operation time, craniotomy as the method of surgery, use of dural substitute, and use of staples for skin closure. Among the diagnoses, operated meningioma was found as a statistically significant risk factor for the development of SSI (Table V). No significant difference was found between operating theatres. Variables found statistically significant in univariate analysis were included in multivariate logistic regression. A significant correlation (Spearman’s R) was found between length of operation time and length of hospital stay. Therefore length of stay was not included in analysis. Results of multivariate modelling are seen in Table VI. The best subsets of variables predicting the development of SSI included dural
Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI.
substitute, operation time, method for skin closure, and surgical method. To illustrate how these are correlated we also did a principal component analysis (see methods) (Fig. 1). This figure shows that staples for skin closure, long surgery time, dural substitute and meningioma are clustered, indicating that they frequently occur together.
Prevalence of surgical site infection The background for our study was that we wanted to define a patient group that could be used for future control of the quality of our routines pertaining to surgical procedures. Therefore we included all patients operated for intracranial tumours, chronic subdural haematomas and reconstructive cranioplasty who were admitted to our post-operative ward. Contrary to other published materials we set a fixed follow-up time of 3 and 12 months. According to CDC as well as Swedish standards, surgery with implants like bone flap fixating material has to be followed up for 12 months in order to rule out infection.10 The prevalence in our study was 4.3% of all procedures after 3 months where 20 of the infections occurred. Another three infections occurred between 3 and 12 months, making the prevalence 4.9% of all procedures. During this time, however, 88 patients from the original group died, making the 12-month prevalence difficult to interpret. Due to the health care organisation we believe that we were
Table IV. This table lists the results from the univariate analysis of risk factors from SSI. No. of operations No. infected % Infected
Admission Time of surgery Diabetes Steroids Blood transfusion Hair removal Wound drainage Method of surgery Dural substitute Wound closure
n.s n.s ⬍ 0.02 ⬍ 0.03
Discussion
Risk factors for infections
Gender
61 years 9.3 persons 13 days 4 h 12 min
258 Men 208 Women 175 Acute 291 Elective 368 Work hours 124 On call 39 Yes 427 No 222 Yes 244 No 54 Yes 411 No 239 Complete 226 Partial 378 Yes 88 No 192 Craniectomy 274 Craniotomy/ 36 Yes 430 No 158 Staples 307 Sutures
15 Men 11 Women 9 Acute 17 Elective 21 Work hours 5 On call 2 Yes 24 No 13 Yes 13 No 4 Yes 22 No 17 Complete 9 Partial 19 Yes 7 No 6 Craniectomy 20 Craniotomy 8 Yes 18 No 14 Staples 12 Sutures
3.2% 2.4% 1.9% 3.6% 4.5% 1.1% 0.4% 5.2% 2.8% 2.8% 0.9% 4.7% 3.7% 1.9% 4.1% 1.5% 1.3% 4.3% 1.7% 3.9% 3.0% 2.6%
p value n.s n.s n.s n.s n.s n.s n.s n.s ⬍ 0.04 ⬍ 0.0003 ⬍ 0.03
Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI, n.s. Not significant.
274 S. Abu Hamdeh et al. Table V. This table lists the results from the univariate analysis of risk factors from SSI. No. of operations No. infected % Infected p value Glioma/Mets Meningioma SDH Cranioplasty Miscellaneous
127 Operations 82 Operations 129 Operations 38 Operations 57 Operations
4 Infections 10 Infections 6 Infections 3 Infections 3 Infections
0.9% 2.3% 1.4% 0.7% 0.7%
n.s ⬍ 0.02 n.s n.s n.s
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Long hospital stay, long duration of the operation, craniotomy as method of surgery, dural substitute, wound closure with staples and the diagnosis of meningioma all significantly increased the risk of SSI.
consulted regarding all cases of SSI, but it cannot be ruled out that there were some more, for example with terminal brain tumours. Our results are in line with other studies that demonstrate an SSI prevalence of 1–11%.1,2,4,10–12 However, most of other published studies describe almost the entire surgical material in one department. Therefore, these other materials are very heterogeneous regarding diagnoses, risk factors and treatments other than surgery. Another large problem is that the follow-up times have varied, ranging from 2 weeks4 to mean 13.5 months.11 Three of the larger studies did not provide any information at all about the follow-up time.2,10,13 It is the latter two of these that reported the lowest incidences of infection. It is therefore difficult to make accurate comparisons between our results and earlier studies. In our material bone flap osteomyelitis was the most common finding, alone or in combination with abscess, subdural empyema or superficial infection. A total of 20/22 patients had cutaneous pathogens as the offending organisms, one of them in combination with Enterococcus fecalis. One had Enterobacter aerogenes only. In another obviously purulent case we had no positive cultures.
Risk factors We found in the univariate analysis that the surgical method craniotomy, use of dural substitute, diagnosis of meningioma, and wound closure with staples were significantly more common in cases with SSI. Longer duration of the surgical procedure was also associated with increased risk for infections. The findings regarding long surgery and implants are consistent with other studies.
Parameters such as dural substitute, diagnosis of meningiomas, and longer surgery frequently occur together as illustrated with principal components analysis (Fig. 1). It is therefore difficult to point out single factor as responsible. We think instead that these parameters indicate a more complicated surgical situation, which increases the possibilities for the wound to be exposed to bacteria. It seems that this situation is more common in surgery of meningiomas in our material. On the other hand, the fact that these variables were selected into the same multivariate model (Table VI) indicates that each has some independent predictive power. Common sense precautions such as reducing door openings, using as non-traumatic techniques as possible and monitoring air quality should be applied, especially during lengthy procedures. Other factors such as hair removal, wound drain, age, gender, number of people in the operating room, diabetes, steroids and blood transfusion were not related to increased risk for SSI. We found that more than 99% of patients received prophylactic antibiotics in accordance with the department’s protocol. The importance of prophylactic antibiotics has been demonstrated earlier.5,11,13 As described in detail by the Surgical Infection Prevention Project it is not enough simply to administer antibiotics; it is necessary to match the type of antibiotic used with the most common cutaneous pathogens, and to optimise timing, redosing and discontinuation.
Impact of SSI Patients who developed SSI required readmission, reoperation and antibiotic therapy in order to control the infection. In 13 cases further surgery was necessary for cranial reconstruction after the infection had been controlled. One patient developed hemiparesis after presenting with subdural empyema. This illustrates the high socio-economic cost of SSI, which was estimated in earlier studies, as well as the patient suffering SSI causes.5
Conclusion In this study we measured the 3- and 12-month prevalence of SSI after 466 craniotomies and craniectomies
Table VI. This table shows the best subsets of variables predicting SSI. Dural substitute stands out as important, in combination with surgery duration and method for skin closure. Degree of Variable 1 Variable 2 Variable 3 Variable 4 freedom AIC L.Ratio Chi2 p value Dural substitute Dural substitute Dural substitute Dural substitute Method of surgery Method of surgery Method of surgery Method of surgery Operation time Skin closure Skin closure Method of surgery Skin closure Skin closure Method of surgery
Operation time Skin closure Skin closure Dural substitute Dural substitute Dural substitute Dural substitute
Operation time Method of surgery Skin closure Skin closure
Operation time Operation time Method of surgery Method of surgery
Operation time
Operation time
1 2 2 3 2 3 3 4 1 2 1 2 3 2 1
170.0146 170.2706 170.3912 171.0302 171.7102 172.2108 172.3870 172.9546 173.8141 173.9941 174.8053 175.6570 175.9274 176.8035 176.8366
7.64083 9.38483 9.26417 10.62518 7.94517 9.44461 9.26838 10.70081 3.84134 5.66132 2.85007 3.99835 5.72802 2.85187 0.81881
⬍ 0.006 ⬍ 0.01 ⬍ 0.01 ⬍ 0.02 ⬍ 0.02 ⬍ 0.03 ⬍ 0.03 ⬍ 0.04 n.s n.s n.s n.s n.s n.s n.s
SSI in standard neurosurgery procedures
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that received postoperative care in the intermediate ward. The SSI prevalence was 4.3% after 3 months. A total of 88 patients died between 3 and 12 months. Only three additional patients (0.8%) developed an SSI during the same 9-month period. Longer surgery time, meningioma, use of dural substitute and skin closure with staples all were significantly associated with the development of SSI after 3 months. Factors contributing to the risk of SSI indicate a more complex surgical situation. These cases require especially stringent safeguards against infection, as well as careful monitoring following surgery in order to detect SSI at an early stage.
Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. O’Keeffe AB, Lawrence T, Bojanic S. Oxford craniotomy infections database: A cost analysis of craniotomy infection. Br J Neurosurg 2012;26:265–9. 2. McClelland S III, Hall WA . Postoperative central nervous system infection: incidence and associated factors in 2111 neurosurgical procedures. Clin Infect Dis 2007;45:55–9.
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3. Dashti SR, Baharvahdat H, Spetzler RF, et al. Operative intracranial infection following craniotomy. Neurosurg Focus 2008;24: E10. 4. Erman T, Demirhindi H, Gocer AI, et al. Risk factors for surgical site infections in neurosurgery patients with antibiotic prophylaxis. Surg Neurol 2005;63:107–112; discussion 112–103. 5. Barker FG II. Efficacy of prophylactic antibiotics for craniotomy: a meta-analysis. Neurosurgery 1994;35:484–90; discussion 491–82. 6. Barker FG II. Efficacy of prophylactic antibiotics against meningitis after craniotomy: a meta-analysis. Neurosurgery 2007;60:887–94; discussion 887–94. 7. Raggueneau JL, Cophignon J, Kind A , et al. [analysis of infectious sequelae of 1000 neurosurgical operations. Effects of prophylactic antibiotherapy]. Neuro-Chirurgie 1983;29:229–33. 8. Horan TC, Andrus M, Dudeck MA . Cdc/nhsn surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309–32. 9. Akaike. A new look at the statistical model identification. IEEE Trans Automat Control 1974;19:716–23. 10. Valentini LG, Casali C, Chatenoud L, et al. Surgical site infections after elective neurosurgery: a survey of 1747 patients. Neurosurgery 2008;62:88–95; discussion 95–86. 11. Blomstedt GC. Infections in neurosurgery: a retrospective study of 1143 patients and 1517 operations. Acta Neurochir 1985;78:81–90. 12. Korinek AM. Risk factors for neurosurgical site infections after craniotomy: a prospective multicenter study of 2944 patients. The french study group of neurosurgical infections, the sehp, and the c-clin paris-nord. Service epidemiologie hygiene et prevention. Neurosurgery 1997;41:1073–9; discussion 1079–81. 13. Korinek AM, Golmard JL, Elcheick A , et al. Risk factors for neurosurgical site infections after craniotomy: a critical reappraisal of antibiotic prophylaxis on 4,578 patients. Br J Neurosurg 2005;19: 155–62.
