Associations between social risk factors and surgical site infections after colectomy and abdominal hysterectomy

IMPORTANCE Surgical site infection (SSI) is an important patient safety outcome. Although social risk factors have been linked to many adverse health outcomes, it is unknown whether such factors are associated with higher rates of SSI. OBJECTIVES To determine whether social risk factors, including race/ethnicity, insurance status, and neighborhood income, are associated with higher rates of SSI after colectomy or abdominal hysterectomy, 2 surgical procedures for which SSI rates are publicly reported and included in pay-forperformance programs by Medicare and other groups. DESIGN, SETTING, AND PARTICIPANTS This cross-sectional study analyzed adults undergoing colectomy or abdominal hysterectomy, as captured in State Inpatient Databases for Arizona, Florida, Iowa, Massachusetts, Maryland, New York, and Vermont. Operations were performed in 2013 through 2014 at general acute care hospitals in the United States. Data analysis was conducted from October 2018 through June 2019. EXPOSURES Colectomy or hysterectomy. MAIN OUTCOMES AND MEASURES Postoperative complex SSI rates. RESULTS A total of 149 741 patients met the inclusion criteria, including 90 210 patients undergoing colectomies (mean [SD] age, 63.4 [15.6] years; 49 029 [54%] female; 74% white, 11% black, 9% Hispanic, and 5% other or unknown race/ethnicity) and 59 531 patients undergoing abdominal hysterectomies (mean [SD] age, 49.8 [11.8] years; 100% female; 52% white, 26% black, 14% Hispanic, and 8% other or unknown race/ethnicity). In the colectomy cohort, 34% had private insurance, 52% had Medicare, 9% had Medicaid, and 5% had other or unknown insurance or were uninsured; 24% were from the lowest quartile of median zip code income. In the hysterectomy cohort, 57% had private insurance, 16% had Medicare, 19% had Medicaid, and 3% had other or unknown insurance or were uninsured; 27% were from the lowest-income zip codes. Within 30 days of surgery, SSI rates were 2.55% for the colectomy cohort and 0.61% for the hysterectomy cohort. For colectomy, black race (adjusted odds ratio [AOR], 0.71; 95% CI, 0.61-0.82) was associated with lower odds of SSI, whereas Medicare (AOR, 1.25; 95% CI, 1.10-1.41), Medicaid (AOR, 1.23; 95% CI, 1.06-1.44), and low neighborhood income (AOR, 1.14; 95% CI, 1.01-1.29) were associated with higher odds of SSI. For hysterectomy, no social risk factors that were examined in this study had statistically significant associations with SSI after adjustment for clinical risk. CONCLUSIONS AND RELEVANCE Inconsistent associations between social risk factors and SSIs were found. For colectomy, infection prevention programs targeting low-income groups may be (continued) Key Points Question Are social risk factors, including race/ethnicity, insurance status, and neighborhood income, associated with higher rates of surgical site infection (SSI) after colectomy or abdominal hysterectomy, 2 surgical procedures for which SSI rates are publicly reported and included in pay-for-performance programs nationally? Findings In this cross-sectional study of 149 741 participants, Medicaid insurance status (a marker for poverty) and living in a low-income zip code were associated with higher SSI rates after colectomy, even after adjusting for clinical risk. For hysterectomy, no social risk factors that were examined in this study had statistically significant associations with SSI after adjustment for clinical risk. Meaning For colectomy, infection prevention programs targeting low-income groups may be important for reducing disparities, and policy makers could consider taking social risk into account when evaluating hospital performance. Author affiliations and article information are listed at the end of this article. Open Access. This is an open access article distributed under the terms of the CC-BY License. JAMA Network Open. 2019;2(10):e1912339. doi:10.1001/jamanetworkopen.2019.12339 (Reprinted) October 2, 2019 1/11 Downloaded From: https://jamanetwork.com/ by a Washington University St Louis User on 02/29/2020 Abstract (continued)continued) important for reducing disparities in this postoperative outcome, and policy makers could consider taking social risk factors into account when evaluating hospital performance. JAMA Network Open. 2019;2(10):e1912339. doi:10.1001/jamanetworkopen.2019.12339


Introduction
Surgical site infections (SSIs) are associated with significant morbidity, mortality, and costs after surgical procedures. 1,2 Complicating up to 5% of surgical procedures nationally, SSIs are common and often preventable. Consequently, reducing SSIs nationally is a priority for patient safety efforts led by The Joint Commission, the Centers for Medicare & Medicaid Services, and consumer organizations such as the Leapfrog Group.
One strategy these organizations have used to encourage reductions in SSI is public reporting of hospital performance. For example, Hospital Compare, Medicare's public reporting website, and the Leapfrog Group publish hospitals' SSI rates for consumers to view. Another strategy to reduce SSI incidence is through the use of financial incentives. For example, Medicare's Hospital-Acquired

Conditions Reduction Program (HACRP), created under the 2010 Patient Protection and Affordable
Care Act, is a pay-for-performance program focused on infections and other adverse safety events. 3 Under this program, 85% of hospitals' performance scores are determined by infection metrics from the Centers for Disease Control and Prevention's National Healthcare Safety Network (NHSN), including complex SSI after colectomy and abdominal hysterectomy. Under the HACRP, hospitals in the worst-performing quartile are penalized 1% of their total Medicare payments, amounting to more than 1 billion dollars in its first 4 years. 3 Consequently, the risk-adjustment methods used for SSI have significant consequences, both in terms of public reputation and financial stability for hospitals. Prior work 4,5 suggests that teaching hospitals and safety-net hospitals are disproportionately penalized under the HACRP, leading to concerns that performance scores may be driven by patient characteristics outside hospitals' control, rather than the quality of care that hospitals deliver. Although the NHSN has recently incorporated diabetes, sex, age, and obesity into their SSI risk adjustment models, no adjustment is made for social risk factors, despite prior studies [6][7][8] showing that social risk factors are associated with an increased risk of infection for other surgical procedures.
Understanding whether social risk factors are associated with SSI for colectomy and abdominal hysterectomy, and whether accounting for these factors would meaningfully change hospitals' performance on these measures, has implications for public reporting and value-based payment models, but has not previously been described, to our knowledge. Therefore, in this study, we aimed to determine whether SSI rates after colectomy or abdominal hysterectomy differ by patient race/ ethnicity, neighborhood income, or insurance type. We also modeled the potential outcomes of accounting for social risk factors on relative performance for safety-net hospitals and teaching hospitals compared with their peers.

Data
Patients undergoing colectomy or abdominal hysterectomy during the years 2013 and 2014 were identified using data from the State Inpatient Databases 9 for Arizona, Florida, Iowa, Massachusetts, Maryland, New York, and Vermont. These states were selected because they allow linkage of individual patients across time, allowing for the ascertainment of postoperative events that happen either during the index hospitalization or after discharge. We identified procedures using International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) procedure  12 Obesity and diabetes were defined as per the Elixhauser Comorbidity Index. 13 We also adjusted for overall

Outcomes
Our primary outcome was the occurrence of a complex SSI. We defined complex SSI as an infection coded during an inpatient hospitalization (index hospitalization or readmission) or requiring operative treatment in an ambulatory surgery facility within 30 days of the index procedure. All other SSIs were categorized as noncomplex and were not outcomes for the purpose of this study.
Complex SSIs were identified using ICD-9-CM diagnosis and procedure codes within 30 days postoperatively, as described elsewhere. 14,15 Briefly, SSIs recorded during the first 30 days after surgical procedures were identified using ICD-9-CM diagnosis codes from encounters in the State Inpatient Databases and State Ambulatory Surgery Databases. 16 Prior work 17,18 in this area has suggested that use of these codes has sensitivity similar to that of routine clinical surveillance for detecting complex SSI, but a lower positive predictive value. We censored the observation period to avoid misclassification of SSIs after a subsequent surgery using the NHSN procedure list, as described elsewhere. 15

Statistical Analysis
Patient characteristics were described using standard statistical tests (χ 2 test and independentsamples t test) as appropriate, and unadjusted complex SSI rates were calculated. We then ran generalized linear models including NHSN risk adjustment elements (estimated ASA risk score of Ն3, age in 10-year increments, sex, diabetes, obesity, and oncology hospital), 12 accounting for clustering by hospital, to examine associations between key risk factors and complex SSIs. We did this in a stepwise manner, such that models first only included each social risk factor alone and subsequently included the NHSN risk adjustment elements and the remainder of the social risk factors.

JAMA Network Open | Surgery
To determine whether adjusting for social risk factors would affect the relative performance of safety-net or teaching hospitals on these measures of complex SSI, we ranked all hospitals performing at least 20 colectomies on their complex SSI rates and assigned percentiles to each. We defined safety-net hospitals as the quintile of hospitals with the greatest proportion of patients with Medicaid health insurance and teaching hospitals as those reporting a medical school affiliation in the American Hospital Association Annual Survey. 11 We ranked all hospitals in order of performance on each complex SSI type and calculated the mean percentile score for safety-net and non-safety-net hospitals, as well as teaching and nonteaching hospitals, using no risk adjustment (raw rates), using current NHSN risk adjustment, and after adding social risk factors to the models. Because higher infection rates are worse, a hospital with a percentile score of 0 would be the best performer and a hospital with a percentile score of 100 would be the worst performer. We also examined the proportion that would be in the worst (highest) quartile of performance under each risk adjustment scenario, because the current HACRP program assigns penalties to hospitals in the worst quartile of performance on a broader set of infection measures.

Patient Population
In total, 149 741 patients met the inclusion criteria, including 90 210 patients undergoing colectomies and 59 531 patients undergoing abdominal hysterectomies ( Table 1). The colectomy cohort had a The hysterectomy cohort was younger, with a mean (SD) age of 49.8 (11.8) years, and all were female. Fourteen percent had an estimated ASA score of 3 or higher, and 18% were coded for obesity.
Fifty-two percent of the sample were white, 26% were black, 14% were Hispanic, and 8% were other or unknown race/ethnicity. The predominant insurer was private insurance (57% of patients), 16% had Medicare, 19% had Medicaid, and 3% had other or unknown insurance or were uninsured; 27% were from the lowest-income zip codes. Within 30 days of surgery, the complex SSI rate was 0.61%.

Association Between Social Risk Factors and Rates and Odds of Complex SSI
For the colectomy cohort, in unadjusted analyses, black race was associated with lower raw rates and  (Figure).
For the hysterectomy cohort, in unadjusted analyses, black race compared with white race (OR,  (Figure).

Discussion
We found that social risk factors were inconsistently associated with complex SSI rates after colectomy or hysterectomy. For colectomy, Medicaid status (a marker for poverty) and living in a low-income zip code were associated with higher complex SSI rates. For hysterectomy, no social risk factors that we examined in this study had statistically significant associations with SSI. Safety-net hospitals performed similarly to non-safety-net hospitals on measures of complex SSI for both colectomy and hysterectomy, and teaching hospitals performed similarly to nonteaching hospitals.
Adding social risk factors to current risk adjustment methods for complex SSI did not change  Adjusted odds ratios (ORs) (squares) and 95% CIs (horizontal lines) for SSI after colectomy (A) and hysterectomy (B).

Limitations
This study has limitations. We relied on billing data for event ascertainment and for risk adjustment and had data for a limited number of states. The NHSN SSI data are drawn from a different set of hospitals nationally, and NHSN surveillance is based on clinical data sourced from primary records and active hospital-level surveillance rather than billing data; therefore, although we are examining the same clinical event, our rates and patterns may not be identical to theirs. Our risk adjustment may also be subject to similar limitations in coding sensitivity for comorbidities as our outcome measure.
Event rates, especially for hysterectomy, were very low, which may suggest limited sensitivity of our analysis for SSI events and likely limited our power in terms of identifying significant associations between social risk factors and our outcome. Our use of an inpatient and ambulatory surgical database to identify events may also contribute to the low observed incidence, because although we expect most complex SSI events included in the outcome to be managed in this setting, some may be managed exclusively in the outpatient setting and, thus, would be excluded from our analysis. This could introduce bias if lower-income populations were more likely to be managed in the outpatient setting, although we are aware of no evidence that this is the case. We simulated percentile ranking to illustrate the outcomes of additional risk adjustment, but the HACRP and other patient safety programs also include other safety measures, so our findings do not directly reflect performance or payment under these programs more broadly. Finally, we had data on only a limited set of social determinants of health, and our negative findings particularly for hysterectomy should not be taken to suggest that no social risk factors are associated with postsurgical outcomes; further research could address additional social risk factors such as education or employment, as well as associated ones such as health literacy.

Conclusions
We found inconsistent associations between social risk and complex SSI. For colectomy, we identified specific patient populations, such as individuals with Medicaid coverage and those in low-income areas, that could be targeted to reduce infection rates. For colectomy, consideration could also be given to adjusting SSI rates for social risk factors in public reporting programs or pay-for-performance programs like the HACRP. The outcomes of patient safety-focused pay-for-performance programs on health care systems serving socially at-risk populations should be closely monitored to identify disparities and opportunities for improvement.