Abstract
Objective
Surgical site infections (SSIs) carry significant patient morbidity and mortality and are a major source of readmissions after craniotomy. Because of their deleterious effects on health care outcomes and costs, identifying modifiable risk factors holds tremendous value. However, because SSIs after craniotomy are rare and most existing data comprise single-institution studies with small sample sizes, many are likely underpowered to discern for such factors. The objective of this study was to use a large hetereogenous patient sample to determine SSI incidence after nonemergent craniotomy and identify factors associated with readmission and subsequent need for wound washout.
Methods
We used the 2010–2014 Nationwide Readmissions Database cohorts to discern for factors predictive of SSI and washout.
Results
We identified 93,920 nonemergent craniotomies. There were 2079 cases of SSI (2.2%) and 835 reoperations for washout (0.89%) within 30 days of index admission and there were 2761 cases of SSI (3.6%) and 1220 reoperations for washout (1.58%) within 90 days. Several factors were predictive of SSI in multivariate analysis, including tumor operations, external ventricular drain (EVD), age, length of stay, diabetes, discharge to an intermediate-care facility, insurance type, and hospital bed size. Many of these factors were similarly implicated in reoperation for washout.
Conclusions
SSI incidence in neurosurgery is low and most readmissions occur within 30 days. Several factors predicted SSI after craniotomy, including operations for tumor, younger age, hospitalization length, diabetes, discharge to institutional care, larger hospital bed size, Medicaid insurance, and presence of an EVD. Diabetes and EVD placement may represent modifiable factors that could be explored in subsequent prospective studies for their associations with cranial SSIs.
Keywords: craniotomy, infection, meningitis, nationwide database, postoperative infection, readmission, surgical site infection (SSI)
Introduction
Surgical site infections (SSIs) are a major concern in neurosurgery given the proximity of the wound to the central nervous system. When they do occur, they carry substantial patient morbidity and mortality with higher resultant length of stays (LOS) and hospital costs 1. SSIs are one of the most common healthcare-associated infections (HAIs) with a fiscal footprint equivalent to roughly $3 billion dollars annually 2. Their reported incidence after craniotomy is variable, ranging from 0.8 to 5.6% 3–9. Various risk factors have been implicated, however, much of the data is inconsistent 3.This is likely attributable to immense variation in study inclusion criteria and SSI definitions employed throughout the literature. Furthermore, as cranial SSIs are considered relatively rare events, many studies are likely underpowered to discern for key predictors of infection 10,11.
Besides antibiotic prophylaxis, no standardized guidelines exist for reducing post-craniotomy SSI 11. Their devastating consequences, coupled with burgeoning healthcare costs and insurers moving away from covering SSIs, mean that identifying modifiable risk factors has ever-increasing value. We therefore queried the newly available Nationwide Readmissions Database (NRD) to elucidate patient, procedure and hospital characteristics associated with readmission for SSI after non-emergent craniotomy. The NRD is a multi-state resource that assigns anonymized linkage numbers, effectively allowing patients to be tracked after discharge throughout the state and within a calendar year. It is unique from other national samples because it is not limited to cross-sectional analysis of hospital admissions. Rather, it affords the ability to longitudinally follow patients after an index admission and to define time-to-event variables (e.g. readmission with SSI). Consequently, the NRD circumvents the issue of different-hospital follow-up inherent to many single-institution investigations, provided follow-up is sought within state lines.
Since postoperative wound complications tend to manifest within the first month of an operation 12, the NRD is ideally suited to analyzing nationwide estimates of SSI. This database has previously been employed in neurosurgery to characterize readmission trends after subarachnoid hemorrhage 13, malignant brain tumor resection 14, stroke 15 and spine surgery 16. Here we report on its use for characterizing SSI after craniotomy. The goals of this investigation were (1) to define 30- and 90-day SSI incidence after non-emergent craniotomy, (2) to determine patient and hospital factors that were predictive of SSI and (3) to characterize factors associated with reoperation for washout.
Methods
Data Source
The 2010–2014 cohorts of the NRD by the Healthcare Cost and Utilization Project (HCUP) were queried for this investigation. The database is comprised of all hospital discharges meeting quality assurance standards from 20–27 member states and approximates 50% of discharges in the US. No IRB/ethics approval was required for use of the publicly available NRD database.
Study Population
Primary inclusion criteria were adults >18 years of age who underwent non-emergent craniotomy. We excluded transphenoidal approaches and craniotomies for trauma, ventricular shunting and deep brain stimulation (DBS) because of the increased risk for infection associated with traversing the nasal passage, emergency cases 6,17 and hardware implantation. The resulting cohort mainly comprised craniotomies for tumor, cerebrovascular disorders and epilepsy. Patients were extracted using the relevant ICD-9CM diagnosis and procedures (Table 1).
Table 1.
International Classification of Diseases, Ninth Edition, Clinical Modification (ICD-9CM) diagnosis and procedures employed for patient extraction from the NRD database
| Craniotomy cohort | Diagnosis code | Procedure code | |
|---|---|---|---|
| Tumor | Benign | 192.1, 225.2, 237.6 | 1.51 |
| 225.1 | 4.01 | ||
| 237.0 | 7.61, 7.64 | ||
| 225.0 | 1.59 | ||
| Malignant | 191.0–191.9 | 1.53, 1.59 | |
| 198.3 | 1.59 | ||
| Vascular | Aneurysm | 430, 437.3 | 39.51 |
| Moya-Moya disease | 437.5 | 39.28 | |
| Cerebro-occlusive disease | 433.00, 433.10, 433.20, 433.30, 433.80, 433.90, 434.10, 434.90, 437.0, 433.01, 433.11, 433.21, 433.31, 433.81, 433.91, 434.01, 434.11, 434.91, 435.x, 437.1 | 39.28 | |
| AVM | 747.81 | 1.59 | |
| Epilepsy | 345.x | 1.53, 1.52 | |
The index admission was defined as the initial hospitalization on which craniotomy was performed. Patients with a diagnosis of SSI (998.30, 998.31, 998.32, 998.5X, 998.83, 998.1x, 998.81, 320.0—322.9, 324.0) on index admission, who died or were missing key data (e.g. LOS or time to procedure) were excluded. From this initial cohort, the NRD was queried for two clinical outcomes at 30- and 90-days: (1) readmission with SSI and (2) readmission with SSI requiring washout (86.22, 01.xx). Because NRD only tracks patients in a single calendar year, those with insufficient time for follow-up were excluded. Hence, for 30-day readmissions only patients discharged between January and November were included and for 90-day readmissions only those discharged between January and September were included.
See Figure 1. for a schematic of study design.
Figure 1.
Schema of study design for analyzing post-craniotomy surgical site infection using the Nationwide Readmission Database
Patient and Hospital Demographics
Various patient and hospital characteristics were included in association analyses with the infectious outcomes of interest. Independent variables associated with the outcome (p < 0.15) in univariate analysis were included in the multiple regression model and stepwise logistic regression employed with caution for confounders. Hospital factors consisted of bed size, teaching status, and annual procedural volume. Craniotomy volume was dichotomized with high volume centers being at or above the 90th percentile per year. Patient factors included: age, gender, insurance, underlying comorbidities, LOS and discharge disposition. Age is present as a continuous variable in the NRD and was categorized as follows for analysis: 18–44, 45–59, 60–74, ≥75. Underlying comorbidities were inferred via the Elixhauser index, which has been dichotomized in the NRD to the presence or absence of a comorbidity. Underlying medical conditions were also queried such as: obesity (278.0, V85.3, V85.4), diabetes (250.xx) and tobacco use (305.1, V15.82). Additionally, clinical factors with the potential to influence SSI were included: extracranial infection (001.00–139.99, 995.91–92), EVD presence (2.21) and ventricular shunt (2.32–2.35).
Statistical Analysis
The primary outcomes were readmission within 30- and 90-days for: (1) SSI, and (2) SSI requiring washout. Readmissions were extracted using standard HCUP methodology. In instances where multiple readmissions were identified, only the first was included for analysis. Multivariable analysis was performed using two-level mixed-effects modeling accounting for clustering and reported using odds ratios (OR) with 95% confidence intervals (CI). Statistical significance was defined as p < 0.05. All analysis was conducted with SAS 9.4 (Cary, NC).
Results
Patient and hospital baseline characteristics
From 2010–2014, there were 93,920 craniotomies that met our inclusion criteria. Most were for tumor (81.2%, n = 76,265) followed by cerebrovascular conditions (17.8%, n = 16,703) and lastly, epilepsy (1%, n = 952). The median LOS for the entire cohort on index admission was 5 days with a median index hospitalization cost of $99,586. The majority of patients were between 45 and 74 years: 18–44 (20.1%), 45–59 (35.2%), 60–74 (34.9%) and ≥75 (9.8%). There was slight female predominance in the index cohort: females (56.4%, n = 52,821) and males (43.6%, n = 41,099). 69% of patients in the index population (n = 64,799) had underlying comorbidities as determined by the Elixhauser index. Most had private (47.2%) or Medicare insurance (33.3%) and were treated at hospitals with large bed size (80.2%).
SSI incidence, readmission demographics
There were 2079 readmissions for SSI within 30 days of index hospitalization, corresponding to an SSI incidence of 2.2% (Table 2). For the cohort readmitted, their median LOS on index admission was 6 days with a median cost of $110,776. The median time to 30-day readmission was 13 days with a median readmission cost of $62,072. Of those readmitted for postoperative infection at 30 days, 40.2% (n = 835) required takeback for wound washout.
Table 2.
Demographics of patients readmitted within 30 days of index hospitalization
| Variables | N | % | |
|---|---|---|---|
| Diagnosis | Malignant Tumor | 1055 | 50.75 |
| Benign Tumor | 745 | 35.83 | |
| Epilepsy | 16 | 0.77 | |
| Vascular | 263 | 12.65 | |
| Total | 2079 | 2.2 | |
| Shunt Procedure | Yes | 32 | 1.54 |
| No | 2047 | 98.46 | |
| Age | 18–44 | 534 | 25.69 |
| 45–59 | 778 | 37.42 | |
| 60–74 | 617 | 29.68 | |
| >=75 | 150 | 7.22 | |
| Gender | Male | 1083 | 52.09 |
| Female | 996 | 47.91 | |
| Primary insurance | Medicare | 602 | 28.96 |
| Medicaid | 329 | 15.82 | |
| Private insurance | 989 | 47.57 | |
| Self-pay | 74 | 3.56 | |
| No charge, Other | 78 | 3.75 | |
| Hospital bedsize | Small | 143 | 6.88 |
| Medium | 290 | 13.95 | |
| Large | 1646 | 79.17 | |
| Teaching Status | Teaching | 1765 | 84.9 |
| Non-Teaching | 314 | 15.1 | |
| Volume | Above 90th percentile | 1185 | 57 |
| <= 90th percentile (97 / year) | 894 | 43 | |
| Disposition | Routine | 1295 | 62.29 |
| Short-term Hospital | 23 | 1.11 | |
| Transfer Other | 361 | 17.36 | |
| Home Health Care | 395 | 19 | |
| Against Medical Advice | DS | DS | |
| Elixhauser comorbidity | Yes | 1462 | 70.32 |
| No | 617 | 29.68 | |
| Medical complication | Yes | 90 | 4.33 |
| No | 1989 | 95.67 | |
| Neurological complication | Yes | 426 | 20.49 |
| No | 1653 | 79.51 | |
| Extra cranial infection | Yes | 186 | 8.95 |
| No | 1893 | 91.05 | |
| Obesity | Yes | DS | DS |
| No | 2070 | 99.57 | |
| Tobacco | Yes | 682 | 32.8 |
| No | 1397 | 67.2 | |
| Diabetes | Yes | 358 | 17.22 |
| No | 1721 | 82.78 | |
| External ventricular drain (EVD) | Yes | 96 | 4.62 |
| No | 1983 | 95.38 | |
| Index Length of Stay | 0–3 days | 572 | 27.51 |
| 4–6 days | 572 | 27.51 | |
| 7–11 days | 449 | 21.6 | |
| >=12 days | 486 | 23.38 | |
| Median household income for patient’s ZIP code, based on current year | 0–25 percentile | 442 | 21.26 |
| 26–50 percentile | 486 | 23.38 | |
| 51–75 percentile | 563 | 27.08 | |
| 541 | 26.02 | ||
DS = Data Suppressed according to HCUP/NRD regulations
Within 90 days, there were 2761 readmissions for SSI, corresponding to a 90-day SSI incidence of 3.6%. The median time to 90-day readmission was 23 days with a median readmission cost of $60,841. Of SSI readmissions, 44.2% (n =1220) required reoperation for washout. See Figure 2.
Figure 2.
Probability of 90-day readmission for SSI (A) and reoperation for washout (B)
Factors associated with SSI within 30- and 90-days
In multivariate models, various procedure-, patient- and hospital-related factors were associated with SSI. We did not subdivide SSI into its various types (e.g. abscess, empyema, wound breakdown) because of the potential for variability in ICD-9 coding across institutions and the fact that the goal of our investigation was to identify modifiable risk factors of infection, which are not likely to differ substantially between the various SSI types. Craniotomy for tumor resection had higher odds for SSI at both 30 days (OR 1.46–1.93, p < 0.0001) and 90 days (OR 1.48–1.83, p < 0.0001) compared to cerebrovascular operations. The latter was used as the reference cohort here due to similarities in operative duration between both groups minus attendant factors that complicate management and that a priori would be expected to increase infection risk (e.g. chemotherapy, radiation). Other procedure-related factors implicated in SSI include the presence of an EVD on index admission. While significant at 30-days (OR 1.33, p =0.01), the association between EVD and SSI was non-significant at 90-days.
Several patient-related factors were predictive for SSI. Younger age correlated with increased likelihood for SSI at 30 and 90 days (OR 2.09–2.15, p < 0.0001), with those aged 18–44 years having more than twice the odds relative to the elderly ( ≥ 75 years). Diabetes also significantly increased the odds of infection at both time points (OR 1.29, p < 0.0001 and 1.23, p = 0.0001) Additional patient-related factors that were predictive for SSI include: male gender, having Medicaid insurance, hospital LOS (greater than 3, but fewer than 11 days) and discharge to an intermediate care facility (e.g. SNF) or with home health care. The relationship between cranial SSI and concomitant extra-cranial infections (pneumonia, urinary tract infections etc.) was explored and found to be non-significant.
Hospital-related factors were evaluated as well, namely teaching status, surgical volume and bed size. Teaching status did not influence likelihood for readmission with SSI. Bed size inversely correlated with SSI, with larger hospitals having lower chances of SSI at 30 and 90 days (OR 0.72–0.74, p < 0.001). Procedural volume held significance at 30-days with high-volume centers (i.e. those above the 90th percentile) carrying an increased risk for SSI (OR 1.16, p = 0.003).
See Tables 3 and 4 for details.
Table 3.
Predictors of 30-day readmissions for SSI by multivariate analysis using survey-adjusted logistic regression
| Variables | Odds Ratio | 95% CI | p-value | ||
|---|---|---|---|---|---|
| Craniotomy cohort | Malignant Tumor | 1.46 | 1.26 | 1.68 | <0.0001 |
| Benign Tumor | 1.93 | 1.66 | 2.24 | <0.0001 | |
| Epilepsy | 0.94 | 0.56 | 1.57 | 0.8066 | |
| Vascular | Ref | ||||
| Age | 18–44 | 2.15 | 1.72 | 2.68 | <.0001 |
| 45–59 | 1.77 | 1.43 | 2.18 | <.0001 | |
| 60–74 | 1.31 | 1.08 | 1.58 | 0.0053 | |
| >=75 | Ref | ||||
| Gender | Male | Ref | |||
| Female | 0.69 | 0.63 | 0.75 | <.0001 | |
| Primary insurance | Medicare | 1.02 | 0.90 | 1.17 | 0.7506 |
| Medicaid | 1.29 | 1.13 | 1.47 | 0.0002 | |
| Self-pay | 1.04 | 0.81 | 1.33 | 0.7836 | |
| No charge, Other | 0.84 | 0.66 | 1.07 | 0.1614 | |
| Private insurance | Ref | ||||
| Hospital bedsize | Small | Ref | |||
| Medium | 0.74 | 0.59 | 0.93 | 0.0087 | |
| Large | 0.72 | 0.59 | 0.87 | 0.0008 | |
| Disposition | Routine | Ref | |||
| Short-term Hospital | 0.91 | 0.59 | 1.41 | 0.6821 | |
| Transfer Other (e.g. SNF) | 1.31 | 1.14 | 1.50 | 0.0001 | |
| Home Health Care | 1.20 | 1.06 | 1.36 | 0.004 | |
| Against Medical Advice | 1.53 | 0.63 | 3.77 | 0.3508 | |
| Procedural volume | Above 90th percentile | 1.16 | 1.05 | 1.29 | 0.0034 |
| <= 90th percentile (115 / year) | Ref | ||||
| Diabetes | Yes | 1.29 | 1.14 | 1.46 | <.0001 |
| No | Ref | ||||
| External ventricular drain (EVD) | Yes | 1.33 | 1.07 | 1.67 | 0.0115 |
| No | Ref | ||||
| Index Length of stay | 0–3 days | Ref | |||
| 4–5 days | 1.21 | 1.07 | 1.38 | 0.0036 | |
| 6–11 days | 1.28 | 1.13 | 1.45 | 0.0001 | |
| >=12 days | 1.12 | 0.97 | 1.29 | 0.1228 | |
| Median household income for patient’s ZIP code, based on current year | 0–25 percentile | Ref | |||
| 26–50 percentile | 1.07 | 0.94 | 1.23 | 0.2883 | |
| 51–75 percentile | 1.09 | 0.96 | 1.24 | 0.1759 | |
| 76–100 percentile | 0.93 | 0.81 | 1.06 | 0.2612 | |
Table 4.
Predictors of 90-day readmissions for SSI by multivariate analysis using survey-adjusted logistic regression
| Variables | Odds Ratio | 95% CI | p-value | ||
|---|---|---|---|---|---|
| Craniotomy cohort | Malignant Tumor | 1.48 | 1.31 | 1.68 | <0.0001 |
| Benign Tumor | 1.83 | 1.61 | 2.08 | <0.0001 | |
| Vascular | Ref | ||||
| Epilepsy | 0.91 | 0.58 | 1.45 | 0.6991 | |
| Age | 18–44 | 2.09 | 1.72 | 2.54 | <.0001 |
| 45–59 | 1.91 | 1.59 | 2.29 | <.0001 | |
| 60–74 | 1.37 | 1.16 | 1.62 | 0.0002 | |
| >=75 | Ref | ||||
| Gender | Male | Ref | |||
| Female | 0.75 | 0.69 | 0.81 | <.0001 | |
| Primary insurance | Medicare | 1.04 | 0.93 | 1.16 | 0.5009 |
| Medicaid | 1.29 | 1.15 | 1.45 | <.0001 | |
| Private insurance | Ref | ||||
| Self-pay | 1.06 | 0.86 | 1.31 | 0.5927 | |
| No charge, Other | 0.91 | 0.75 | 1.11 | 0.3715 | |
| Disposition | Routine | Ref | |||
| Short-term Hospital | 1.00 | 0.69 | 1.45 | 0.9915 | |
| Transfer Other (e.g. SNF) | 1.39 | 1.23 | 1.56 | <.0001 | |
| Home Health Care | 1.18 | 1.05 | 1.31 | 0.0036 | |
| Against Medical Advice | 2.15 | 1.08 | 4.27 | 0.029 | |
| Diabetes | Yes | 1.23 | 1.10 | 1.37 | 0.0001 |
| No | Ref | ||||
| Hospital bedsize | Small | Ref | |||
| Medium | 0.75 | 0.61 | 0.91 | 0.0032 | |
| Large | 0.74 | 0.62 | 0.88 | 0.0005 | |
| Index Length of stay | 0–3 days | Ref | |||
| 4–5 days | 1.10 | 0.99 | 1.23 | 0.082 | |
| 6–11 days | 1.11 | 1.00 | 1.24 | 0.056 | |
| >=12 days | 0.98 | 0.86 | 1.10 | 0.6868 | |
Factors associated with reoperation for washout within 30- and 90- days
Many of the factors associated with SSI were again implicated in reoperation for wound washout. Significant predictors at 30- and 90- days, respectively, include: craniotomy for tumor (OR 1.91–2.06, p < 0.0001 and 1.72–2.01, p < 0.0001), discharge to intermediate care facility (OR 1.41, p = 0.0007 and OR 1.44, p < 0.0001), discharge with home health care (OR 1.43, p < 0.0001 and 1.27, p = 0.002), younger age and male gender. Diabetes (OR 1.39, p = 0.0005), presence of EVD during index hospitalization (OR 1.47, p = 0.02), having Medicaid insurance (OR 1.30, p = 0.01) and high procedural volume (OR 1.19, p = 0.02) correlated with reoperation for washout within 30-days, but were not significant at 90-days.
See Tables 5 and 6 for details.
Table 5.
Predictors of 30-day readmissions for SSI requiring reoperation for washout by multivariate analysis using survey-adjusted logistic regression
| Variables | Odds Ratio | 95% CI | p-value | ||
|---|---|---|---|---|---|
| Craniotomy cohort | Malignant Tumor | 1.91 | 1.51 | 2.41 | <0.0001 |
| Benign Tumor | 2.06 | 1.61 | 2.63 | <.0001 | |
| Epilepsy | 1.73 | 0.89 | 3.37 | 0.1042 | |
| Vascular | Ref | ||||
| Age | 18–44 | 2.62 | 1.82 | 3.75 | <.0001 |
| 45–59 | 2.22 | 1.57 | 3.13 | <.0001 | |
| 60–74 | 1.57 | 1.14 | 2.14 | 0.0051 | |
| >=75 | Ref | ||||
| Gender | Male | Ref | |||
| Female | 0.66 | 0.58 | 0.76 | <.0001 | |
| Primary insurance | Medicare | 1.00 | 0.82 | 1.23 | 0.9812 |
| Medicaid | 1.30 | 1.06 | 1.59 | 0.0104 | |
| Private insurance | Ref | ||||
| Self-pay | 1.14 | 0.79 | 1.65 | 0.4731 | |
| No charge, Other | 0.72 | 0.48 | 1.07 | 0.1023 | |
| Disposition | Routine | Ref | |||
| Short-term Hospital | 0.44 | 0.16 | 1.18 | 0.1017 | |
| Transfer Other (e.g. SNF) | 1.41 | 1.16 | 1.73 | 0.0007 | |
| Home Health Care | 1.43 | 1.19 | 1.70 | <.0001 | |
| Against Medical Advice | 1.52 | 0.37 | 6.19 | 0.5569 | |
| Volume | Above 90th percentile | 1.19 | 1.02 | 1.38 | 0.0247 |
| <= 90th percentile (115 / year) | Ref | ||||
| Diabetes | Yes | 1.39 | 1.15 | 1.67 | 0.0005 |
| No | Ref | ||||
| External ventricular drain (EVD) | Yes | 1.47 | 1.06 | 2.04 | 0.0227 |
| No | Ref | ||||
Table 6.
Predictors of 90-day readmissions for SSI requiring reoperation for washout by multivariate analysis using survey-adjusted logistic regression
| Variables | Odds Ratio | 95% CI | p-value | ||
|---|---|---|---|---|---|
| Craniotomy cohort | Malignant Tumor | 1.721 | 1.421 | 2.084 | <0.0001 |
| Benign Tumor | 2.012 | 1.65 | 2.454 | <0.0001 | |
| Vascular | Ref | ||||
| Epilepsy | 1.294 | 0.693 | 2.415 | 0.4181 | |
| Age | 18–44 | 2.374 | 1.826 | 3.087 | <.0001 |
| 45–59 | 2.162 | 1.689 | 2.769 | <.0001 | |
| 60–74 | 1.473 | 1.15 | 1.887 | 0.0022 | |
| >=75 | Ref | ||||
| Gender | Male | Ref | |||
| Female | 0.69 | 0.614 | 0.774 | <.0001 | |
| Disposition | Routine | Ref | |||
| Short-term Hospital | 0.672 | 0.345 | 1.308 | 0.2418 | |
| Transfer Other (e.g. SNF) | 1.444 | 1.229 | 1.698 | <.0001 | |
| Home Health Care | 1.272 | 1.091 | 1.482 | 0.0021 | |
| Against Medical Advice | 2.167 | 0.793 | 5.919 | 0.1316 | |
| Diabetes | Yes | 1.156 | 0.986 | 1.357 | 0.0744 |
| No | Ref | ||||
Discussion
Hospital readmissions are a substantial burden on healthcare expenditure, accounting for 20% of Medicare payments 18. In an era of value-based Medicine where reimbursement is increasingly being linked to performance and quality of care, reducing unplanned readmissions has become a central focus of hospital administrators and policymakers. SSIs are a major culprit behind unplanned readmissions and are associated with unwanted sequelae including reoperation, prolonged LOS and added patient morbidity, if not mortality 19. Their true cost is borne out not only in higher hospital charges, but in lost economic productivity from delays in return to the workforce. In light of these ramifications, and SSIs being viewed as a litmus test for surgeon and hospital quality, identifying modifiable risk factors is of paramount importance. We therefore queried the NRD database to elucidate patient and hospital characteristics that influence readmissions for SSI and reoperation for washout.
Cranial neurosurgery generally has a low SSI incidence 10. For example, a retrospective study from one of the highest volume neurosurgical centers in North America found only 82 cases of infection requiring reoperation among 16,450 cranial surgeries performed between January 1997 and December 2007 11. Because of the small number of infections, sample sizes thus have to be fairly large in order to generate an accurate estimate of SSI incidence and even larger to discern for predictors of infection 10. Prospective studies, which generally span shorter time intervals, fare even worse and multicenter analyses on SSI are sparse 20. The NRD provides a large heterogeneous sample of patients, circumventing this issue of sample size. Moreover, it provides the unique ability to track patients within a state regardless of the hospital at which care is rendered. This is particularly useful in studying post-craniotomy SSI since the urgent nature of the diagnosis often dictates that patients present to the nearest, rather than the original, treatment facility.
In our study, the overall SSI incidence among non-emergent craniotomies was 2.2% at 30 days and 3.6% at 90 days. These figures are on the lower end of the spectrum (0.8–5.6%) reported by single-institution retrospective and prospective studies 3–9, but in line with values published by other national database investigations (1.8–2.04%) 17,21. The former can partly be attributed to the shorter follow-up specified in our analysis vis-à-vis the much longer period—years to decades—over which many single-institution studies are conducted. Additionally, we determined the rate of SSI takeback for washout to be 0.89% and 1.58% at 30- and 90 days, respectively. These values are also in agreement with the existing literature 11.
Craniotomies for tumor were independently associated with readmission for postoperative infection and need for washout. This relationship has previously been described by others 22,23. One explanation for this finding is that these patients are more likely to have had recent exposure to radiation therapy or pharmacotherapies (e.g. chemotherapy, steroids) that might reasonably be expected to compromise wound healing. Other procedure-related factors that significantly correlated with SSI in our study include presence of an EVD on index admission. EVDs have been implicated in neurosurgical SSIs many times throughout the literature 8,9,24–26. This is not surprising given the potential for drain colonization with seeding of bacteria into the CSF and deeper CNS. These data intimate that close vigilance be maintained for infection throughout the perioperative period, particularly when patients have undergone surgery for tumor and have an EVD in place. Current neurocritical care guidelines do not advocate for antibiotic prophylaxis beyond a single dose at the time of insertion 27.However, further studies may offer opportunity to expand upon our findings, perhaps exploring both duration of EVD placement and utility of routine CSF surveillance.
It is well known that diabetes mellitus (DM) figures prominently as a key player in SSI 28–30. However, data addressing the role of diabetes in cranial neurosurgery are conflicting. Some studies suggest a correlation between the two 17. Others have found no relationship whatsoever 21. And yet still, others suggest that it is the presence of intraoperative hyperglycemia at the time of craniotomy rather than a history of underlying DM that predisposes to SSI 31. We found diabetes to be a significant predictor for both SSI and takeback for washout. These results advocate for optimal DM control, especially in scenarios where delay of the craniotomy would not otherwise cause irreparable harm.
Discharge with home health care or to an intermediate care facility (e.g. SNF) were also significant predictors of infection and washout. Discharge to an intermediate care facility implies that patients have not achieved their pre-morbid functional state and thus require additional resources to meet their needs. It is plausible then that there are greater lapses in local wound care in the context of such diminished functionality, ultimately predisposing to SSI. Furthermore, extra-cranial infections (e.g. UTIs, pneumonia) are quite common in intermediate care facilities with a high prevalence of colonization by antimicrobial-resistant organisms among residents 32. These could serve as a source for secondary seeding of the surgical site through systemic spread. The higher rates of SSI in patients discharged to intermediate care facilities indicate that a high index of suspicion should be maintained in this cohort perhaps by scheduling earlier and more frequent office visits in the immediate postoperative period.
Younger age also had a significant association with readmission for SSI and washout in our multivariate analyses. Both older age 17,33,34 and younger age 7,21 have been directly correlated with SSI risk following neurosurgery. One putative explanation for the inverse relationship between age and SSI we observed is that older patients (i.e. ≥75 years) might be less likely to undergo complex surgeries with protracted operative times, which are an independent risk factor for SSI. Hardy et al have shown that for each additional hour spent in a craniotomy for tumor resection, the odds of infection increased by 43% 35. Because the NRD does not provide details regarding operative length, we are unable to adjust for multiple confounders associated with this variable.
There is a growing body of evidence demonstrating inferior outcomes and higher complication rates among patients with public insurance relative to those with commercial insurance 14,36–39. We found that patients with Medicaid were more likely to get readmitted for SSI and undergo reoperation for washout. Similar findings have been reported in spine surgery by Manoso et al, in which Medicaid payer status conferred twice the risk of SSI compared to the privately insured 40. Why Medicaid status results in poorer clinical outcomes likely has to do with these patients having poorer baseline health, more limited access to providers and unreasonable out-of-pocket expenses that decrease treatment compliance 40. This observation has given rise to the concept of ‘underinsurance’ 41,42 with some suggesting that it is as big a challenge to public health as having no insurance at all 43. Because there are 74 million Medicaid enrollees 44, one concern here is that higher complication rates among this subset of patients could lead to the institutions that care for them being unfairly penalized under value-based reimbursement models. Ultimately, this could have the unintended consequence of further limiting access to care, as institutions place caps on the number of patients treated with Medicaid. This relationship between Medicaid and SSI deserves further investigation.
Limitations are inherent in this study. First, NRD only tracks patients within a single calendar year. Consequently, 30- and 90-day readmissions exclude data beyond November and September, respectively. This has the potential to underestimate SSI incidence, particularly any seasonality effects on infection. Second, NRD does not afford the ability to track patients across state lines, which could skew readmission figures in an era where patients often travel outside their home state for care at specialized centers. Third, NRD specifically censors important demographic variables like race that would have allowed for more detailed socioeconomic analyses. Additionally, there are concerns that would apply to any database study such as clerical errors during data entry, ICD-9 miscoding and incomplete hospital records. Because the user does not have access to patient records or clinical outcomes, there is no way to formally validate the information extracted with actual patient data. Nonetheless, the NRD has been extensively employed throughout the literature as a tool for exploring readmission trends across a wide range of subspecialties 45–49.
Conclusions
Using the newly available NRD we determined the incidence of SSI after non-emergent craniotomy to be 2.2% at 30 days and 3.6% at 90 days. Various patient-, procedure- and hospital-related factors were significant predictors of SSI. They include craniotomy for tumor, EVD presence, younger age, LOS, diabetes, patient disposition to an intermediate-care facility (e.g. SNF), Medicaid insurance and large hospital bed size. Many of these factors were similarly linked to subsequent reoperation for washout. Detailed randomized prospective studies may be warranted to evaluate modifiable risk factors such as EVD placement and diabetes and their associations with infection. Furthermore, the relationship between Medicaid insurance and SSI is novel and merits further investigation since it suggests that hospitals may be unfairly penalized under value-based healthcare reimbursement models.
Acknowledgments
Disclosure of Funding: None
Abbreviations
- NRD
Nationwide Readmissions Database
- ICD-9CM
International Classification of Diseases, Ninth Edition, Clinical Modification
- SSI
surgical site infection
- HAI
healthcare associated infection
- EVD
external ventricular drain
- SNF
skilled nursing facility
- DBS
deep brain stimulation
- CSF
cerebrospinal fluid
- CNS
central nervous system
Footnotes
Conflict of Interest: The authors have no conflicts of interest to disclose
References
- 1.O’Keeffe AB, Lawrence T, Bojanic S. Oxford craniotomy infections database: a cost analysis of craniotomy infection. Br J Neurosurg. 2012;26(2):265–269. [DOI] [PubMed] [Google Scholar]
- 2.Hidron AI, Edwards JR, Patel J, et al. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol. 2008;29(11):996–1011. [DOI] [PubMed] [Google Scholar]
- 3.Cassir N, De La Rosa S, Melot A, et al. Risk factors for surgical site infections after neurosurgery: A focus on the postoperative period. Am J Infect Control. 2015;43(12):1288–1291. [DOI] [PubMed] [Google Scholar]
- 4.Abu Hamdeh S, Lytsy B, Ronne-Engstrom E. Surgical site infections in standard neurosurgery procedures- a study of incidence, impact and potential risk factors. Br J Neurosurg. 2014;28(2):270–275. [DOI] [PubMed] [Google Scholar]
- 5.McClelland S 3rd, Hall WA. Postoperative central nervous system infection: incidence and associated factors in 2111 neurosurgical procedures. Clin Infect Dis. 2007;45(1):55–59. [DOI] [PubMed] [Google Scholar]
- 6.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(5):1073–1079; discussion 1079–1081. [DOI] [PubMed] [Google Scholar]
- 7.Valentini LG, Casali C, Chatenoud L, Chiaffarino F, Uberti-Foppa C, Broggi G. Surgical site infections after elective neurosurgery: a survey of 1747 patients. Neurosurgery. 2008;62(1):88–95; discussion 95–86. [DOI] [PubMed] [Google Scholar]
- 8.Sneh-Arbib O, Shiferstein A, Dagan N, et al. Surgical site infections following craniotomy focusing on possible post-operative acquisition of infection: prospective cohort study. Eur J Clin Microbiol Infect Dis. 2013;32(12):1511–1516. [DOI] [PubMed] [Google Scholar]
- 9.Kourbeti IS, Vakis AF, Ziakas P, et al. Infections in patients undergoing craniotomy: risk factors associated with post-craniotomy meningitis. J Neurosurg. 2015;122(5):1113–1119. [DOI] [PubMed] [Google Scholar]
- 10.Walcott BP, Redjal N, Coumans JV. Infection following operations on the central nervous system: deconstructing the myth of the sterile field. Neurosurg Focus. 2012;33(5):E8. [DOI] [PubMed] [Google Scholar]
- 11.Dashti SR, Baharvahdat H, Spetzler RF, et al. Operative intracranial infection following craniotomy. Neurosurg Focus. 2008;24(6):E10. [DOI] [PubMed] [Google Scholar]
- 12.Buckwold FJ, Hand R, Hansebout RR. Hospital-acquired bacterial meningitis in neurosurgical patients. J Neurosurg. 1977;46(4):494–500. [DOI] [PubMed] [Google Scholar]
- 13.Rumalla K, Smith KA, Arnold PM, Mittal MK. Subarachnoid Hemorrhage and Readmissions: National Rates, Causes, Risk Factors, and Outcomes in 16,001 Hospitalized Patients. World Neurosurg. 2017. [DOI] [PubMed] [Google Scholar]
- 14.Donoho DA, Wen T, Babadjouni RM, et al. Predictors of 30- and 90-day readmission following craniotomy for malignant brain tumors: analysis of nationwide data. J Neurooncol. 2018;136(1):87–94. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Vahidy FS, Donnelly JP, McCullough LD, et al. Nationwide Estimates of 30-Day Readmission in Patients With Ischemic Stroke. Stroke. 2017;48(5):1386–1388. [DOI] [PubMed] [Google Scholar]
- 16.Rumalla K, Smith KA, Arnold PM. National Rates, Causes, Risk Factors, and Outcomes Associated With 30-Day and 90-Day Readmissions Following Degenerative Posterior Cervical Spine Surgery Utilizing the Nationwide Readmissions Database. Neurosurgery. 2017;81(5):740–751. [DOI] [PubMed] [Google Scholar]
- 17.Karhade AV, Cote DJ, Larsen AM, Smith TR. Neurosurgical Infection Rates and Risk Factors: A National Surgical Quality Improvement Program Analysis of 132,000 Patients, 2006–2014. World Neurosurg. 2017;97:205–212. [DOI] [PubMed] [Google Scholar]
- 18.Jencks SF, Williams MV, Coleman EA. Rehospitalizations among patients in the Medicare fee-for-service program. N Engl J Med. 2009;360(14):1418–1428. [DOI] [PubMed] [Google Scholar]
- 19.Plowman R The socioeconomic burden of hospital acquired infection. Euro Surveill. 2000;5(4):49–50. [DOI] [PubMed] [Google Scholar]
- 20.Lietard C, Thebaud V, Besson G, Lejeune B. Risk factors for neurosurgical site infections: an 18-month prospective survey. J Neurosurg. 2008;109(4):729–734. [DOI] [PubMed] [Google Scholar]
- 21.McCutcheon BA, Ubl DS, Babu M, et al. Predictors of Surgical Site Infection Following Craniotomy for Intracranial Neoplasms: An Analysis of Prospectively Collected Data in the American College of Surgeons National Surgical Quality Improvement Program Database. World Neurosurg. 2016;88:350–358. [DOI] [PubMed] [Google Scholar]
- 22.Chiang HY, Kamath AS, Pottinger JM, et al. Risk factors and outcomes associated with surgical site infections after craniotomy or craniectomy. J Neurosurg. 2014;120(2):509–521. [DOI] [PubMed] [Google Scholar]
- 23.Tenney JH, Vlahov D, Salcman M, Ducker TB. Wide variation in risk of wound infection following clean neurosurgery. Implications for perioperative antibiotic prophylaxis. J Neurosurg. 1985;62(2):243–247. [DOI] [PubMed] [Google Scholar]
- 24.Camacho EF, Boszczowski I, Basso M, et al. Infection rate and risk factors associated with infections related to external ventricular drain. Infection. 2011;39(1):47–51. [DOI] [PubMed] [Google Scholar]
- 25.Hetem DJ, Woerdeman PA, Bonten MJ, Ekkelenkamp MB. Relationship between bacterial colonization of external cerebrospinal fluid drains and secondary meningitis: a retrospective analysis of an 8-year period. J Neurosurg. 2010;113(6):1309–1313. [DOI] [PubMed] [Google Scholar]
- 26.Lo CH, Spelman D, Bailey M, Cooper DJ, Rosenfeld JV, Brecknell JE. External ventricular drain infections are independent of drain duration: an argument against elective revision. J Neurosurg. 2007;106(3):378–383. [DOI] [PubMed] [Google Scholar]
- 27.Mehta AI, Babu R, Karikari IO, et al. 2012 Young Investigator Award winner: The distribution of body mass as a significant risk factor for lumbar spinal fusion postoperative infections. Spine (Phila Pa 1976). 2012;37(19):1652–1656. [DOI] [PubMed] [Google Scholar]
- 28.Zhang Y, Zheng QJ, Wang S, et al. Diabetes mellitus is associated with increased risk of surgical site infections: A meta-analysis of prospective cohort studies. Am J Infect Control. 2015;43(8):810–815. [DOI] [PubMed] [Google Scholar]
- 29.Finney SJ, Zekveld C, Elia A, Evans TW. Glucose control and mortality in critically ill patients. JAMA. 2003;290(15):2041–2047. [DOI] [PubMed] [Google Scholar]
- 30.Furnary AP, Zerr KJ, Grunkemeier GL, Starr A. Continuous intravenous insulin infusion reduces the incidence of deep sternal wound infection in diabetic patients after cardiac surgical procedures. Ann Thorac Surg. 1999;67(2):352–360; discussion 360–352. [DOI] [PubMed] [Google Scholar]
- 31.Gruenbaum SE, Toscani L, Fomberstein KM, et al. Severe Intraoperative Hyperglycemia Is Independently Associated With Postoperative Composite Infection After Craniotomy: An Observational Study. Anesth Analg. 2017;125(2):556–561. [DOI] [PubMed] [Google Scholar]
- 32.Nicolle LE. Infection control in long-term care facilities. Clin Infect Dis. 2000;31(3):752–756. [DOI] [PubMed] [Google Scholar]
- 33.Erman T, Demirhindi H, Gocer AI, Tuna M, Ildan F, Boyar B. Risk factors for surgical site infections in neurosurgery patients with antibiotic prophylaxis. Surg Neurol. 2005;63(2):107–112; discussion 112–103. [DOI] [PubMed] [Google Scholar]
- 34.Shinoura N, Yamada R, Okamoto K, Nakamura O. Early prediction of infection after craniotomy for brain tumours. Br J Neurosurg. 2004;18(6):598–603. [DOI] [PubMed] [Google Scholar]
- 35.Hardy SJ, Nowacki AS, Bertin M, Weil RJ. Absence of an association between glucose levels and surgical site infections in patients undergoing craniotomies for brain tumors. J Neurosurg. 2010;113(2):161–166. [DOI] [PubMed] [Google Scholar]
- 36.Dasenbrock HH, Wolinsky JP, Sciubba DM, Witham TF, Gokaslan ZL, Bydon A. The impact of insurance status on outcomes after surgery for spinal metastases. Cancer. 2012;118(19):4833–4841. [DOI] [PubMed] [Google Scholar]
- 37.Kapoor JR, Kapoor R, Hellkamp AS, Hernandez AF, Heidenreich PA, Fonarow GC. Payment source, quality of care, and outcomes in patients hospitalized with heart failure. J Am Coll Cardiol. 2011;58(14):1465–1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Kwok J, Langevin SM, Argiris A, Grandis JR, Gooding WE, Taioli E. The impact of health insurance status on the survival of patients with head and neck cancer. Cancer. 2010;116(2):476–485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Shen JJ, Washington EL. Disparities in outcomes among patients with stroke associated with insurance status. Stroke. 2007;38(3):1010–1016. [DOI] [PubMed] [Google Scholar]
- 40.Manoso MW, Cizik AM, Bransford RJ, Bellabarba C, Chapman J, Lee MJ. Medicaid status is associated with higher surgical site infection rates after spine surgery. Spine (Phila Pa 1976). 2014;39(20):1707–1713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Bodenheimer T Underinsurance in America. N Engl J Med. 1992;327(4):274–278. [DOI] [PubMed] [Google Scholar]
- 42.Bashshur R, Smith DG, Stiles RA. Defining underinsurance: a conceptual framework for policy and empirical analysis. Med Care Rev. 1993;50(2):199–218. [DOI] [PubMed] [Google Scholar]
- 43.Link CL, McKinlay JB. Only half the problem is being addressed: underinsurance is as big a problem as uninsurance. Int J Health Serv. 2010;40(3):507–523. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.www.medicaid.gov. Medicaid and CHIP Enrollment Data. www.medicaid.gov. Accessed 1/1/2018, 2018.
- 45.Markham JL, Hall M, Gay JC, Bettenhausen JL, Berry JG. Length of Stay and Cost of Pediatric Readmissions. Pediatrics. 2018;141(4). [DOI] [PubMed] [Google Scholar]
- 46.Smilowitz NR, Beckman JA, Sherman SE, Berger JS. Hospital Readmission After Perioperative Acute Myocardial Infarction Associated With Noncardiac Surgery. Circulation. 2018;137(22):2332–2339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Zafar SN, Shah AA, Channa H, Raoof M, Wilson L, Wasif N. Comparison of Rates and Outcomes of Readmission to Index vs Nonindex Hospitals After Major Cancer Surgery. JAMA Surg. 2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Babadjouni R, Wen T, Donoho DA, et al. Increased Hospital Surgical Volume Reduces Rate of 30- and 90-Day Readmission After Acoustic Neuroma Surgery. Neurosurgery. 2018. [DOI] [PubMed] [Google Scholar]
- 49.Veeranki SP, Sharma K, Ohabughiro MU, et al. 30-Day Readmissions in Hospitalized Adults With Asthma Exacerbations: Insights From the Nationwide Readmission Database. Chest. 2016;150(5):1162–1165. [DOI] [PubMed] [Google Scholar]


