Sepsis

Occurrence and outcomes of sepsis: Influence of race* Viktor Y. Dombrovskiy, MD, PhD, MPH; Andrew A. Martin, MD; Jagadeeshan Sunderram, MD; Harold L. Paz, MD Objective: To evaluate premorbid conditions and sociodemographic characteristics associated with differences in hospitalization and mortality rates of sepsis in blacks and whites. Design: Secondary data analysis of the publicly available New Jersey State Inpatient Database for 2002. Setting: Acute care hospitals in New Jersey. Patients: All black and white adult patients with sepsis hospitalized in 2002. Interventions: None. Measurements and Main Results: A total of 5,466 black and 19,373 white adult patients with sepsis were identified with the International Classification of Diseases, Ninth Revision, Clinical Modification codes for septicemia. Blacks were significantly younger than whites (61.6 0.25 and 72.8 0.11 yrs, respectively, p < .0001). Blacks had greater hospitalization rates than whites, with the greatest disparity between the ages of 35 and 44 yrs (relative risk, 4.35; 95% confidence interval, 3.93– 4.82). Compared with whites, blacks had higher age-adjusted rates for hospitalization and mortality but similar case fatality rates. They were more likely than whites to be admitted to the hospital through the emergency room (odds ratio, 1.4; 95% confidence interval, 1.27–1.50) and to the intensive care unit (odds ratio, 1.14; 95% confidence interval, 1.07–1.21), and they were 3.96 times (95% confidence interval, 3.44 – 4.56) more likely to be uninsured. Black patients with sepsis had a greater likelihood of human immunodeficiency virus infection, diabetes, obesity, burns, and chronic renal failure than white patients and had a smaller likelihood of cancer, trauma, and urinary tract infection. Conclusions: In this study, age-adjusted case fatality rates for hospitalized white and black patients with sepsis were similar. These data are not suggestive of systematic disparities in the quality of treatment of sepsis between blacks and whites. However, blacks had higher rates of hospitalization and population-based mortality for sepsis. We speculate that disparities in disease prevention and care of preexisting conditions before sepsis onset may explain these differences. (Crit Care Med 2007; 35:763–768) KEY WORDS: sepsis; critical care; population groups; hospitalization; mortality; case fatality D espite decades of biomedical research and significant improvements in medical management, sepsis remains among the ten leading causes of death in the United States (1). In fact, the incidence of sepsis has increased over time, and the severity of disease and resource utilization has escalated (2– 6). The results of several epidemiologic studies in the United States indicate a higher level of hospitalization and mortality due to sepsis in blacks compared with whites (3, 5, 7–10). In an earlier study examining the trends in hospitalization, mor- tality, and case fatality from 1995 to 2002, we found similar differences (11). These findings are of great interest and practical importance, but previous studies have not examined in detail the co-morbidities and sociodemographic factors related to these differences. We hypothesized that racial discrepancies in rates of sepsis hospitalization are associated with differences in the prevalence of premorbid conditions and insurance status. Therefore, we examined premorbid conditions, demographic factors, and insurance status in black and white patients with sepsis hospitalized in New Jersey in 2002. MATERIALS AND METHODS *See also p. 958. From the Division of Pulmonary and Critical Care Medicine, Department of Medicine, UMDNJ–Robert Wood Johnson Medical School, New Brunswick, NJ (VYD, AAM, JS); and Pennsylvania State University College of Medicine, Hershey, PA (HLP). Dr. Paz is a consultant/advisor for Johnson and Johnson. The remaining authors have not disclosed any potential conflicts or interest. Copyright © 2007 by the Society of Critical Care Medicine and Lippincott Williams & Wilkins DOI: 10.1097/01.CCM.0000256726.80998.BF Data Sources. We conducted a secondary data analysis of the publicly available New Jersey State Inpatient Database that was developed as part of the Healthcare Cost and Utilization Project, sponsored by the Agency for Healthcare Research and Quality, and included the universe of the inpatient discharge abstracts in the state. The New Jersey State Inpatient Database is based on the files with the hospital inpatient discharge records, created by the New Jersey Department of Health and Senior Services, which maintains statewide data systems and has partnered with the Agency for Healthcare Research and Quality. In 2002, this database contained 1,153,654 observations and 175 clinical and nonclinical variables included in a hospital discharge abstract. We restricted our data to sepsis cases in white and black adults ( 18 yrs old) and variables recognizing patient demographics (age, sex, and race), principal and secondary diagnoses, principal and secondary procedures, admission and discharge status, payment source (Medicare, Medicaid, private insurance, selfpay, and other), and unit of service. Principal and nine secondary diagnoses and principal and seven secondary procedures in the New Jersey State Inpatient Database 2002 are coded both with International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes and Clinical Classification Software codes. The latter consolidates numerous diagnoses and procedures with ICD9-CM codes into a limited number of clinical categories. Study Population. All adult inpatients with sepsis in New Jersey in 2002 were identified with the ICD-9-CM diagnostic codes that were described in our earlier study (11). To identify some coexisting conditions, we used the following Clinical Classification Software codes: Crit Care Med 2007 Vol. 35, No. 3 763 5, for human immunodeficiency virus (HIV) infection; 11– 43, for cancer; 158, for chronic renal failure; 159, for urinary tract infection; 225–236, for trauma; and 240, for burns. Diabetes mellitus was identified by ICD-9-CM codes 250.0 –250.9, with fifth-digits 1 and 3 for type I, and 0 and 2 for type II. To identify obesity, we used ICD-9-CM codes 278.00, 278.01, and V77.8. Statistical Analysis. To evaluate population-based rates of hospitalization and mortality for patients with sepsis, we used the U.S. Census Bureau age-, sex-, and race-specific population estimates for New Jersey in 2002 as denominators and calculated these rates as the number of events per 100,000 population. The same data in association with the hospitalization data were used for computing of relative risk of sepsis in the black vs. white population. The case fatality rate for sepsis was defined as the number of patients with sepsis who died in the hospital divided by the number of all hospitalized patients with sepsis multiplied by 100. Because sepsis incidence increases with age, the effect of age differences in the structure of white and black populations should be eliminated when comparing race-specific rates. For this purpose, we adjusted all racespecific rates by age calculating the direct standardized rate with the standard error (12). The structure of the New Jersey Census 2000 population was used as a standard while computing standardized hospitalization and mortality rates; the structure of the hospitalized population in 2002 in New Jersey was employed as a standard to calculate standardized rate of case fatality. SAS 9.1.2 software (SAS Institute, Cary, NC) was utilized for the analysis of the database and all statistics. To test the difference between groups, we used chi-square analysis for categorical variables, Student’s t-test for continuous values, and z-ratio with p value for two independent proportions. All reported p values are two-sided. The study was approved by the Institutional Review Board of the University of Medicine and Dentistry of New Jersey–Robert Wood Johnson Medical School. Table 1. Characteristics of patients with sepsis Characteristic Total Men Women ICU admissions, total Men Women Age, yrs 18–34 35–44 45–54 55–64 65–74 75–84 85 Coexisting conditions HIV infection Cancer Trauma Burns Diabetes mellitus Type I Type II Obesity Chronic renal failure Urinary tract infection Primary payor Medicare Medicaid Private Self-pay Other Whites, n (%) 19373 (78.0) 9016 (46.5) 10357 (53.5) 7204 (37.2) 3538 (39.2) 3666 (35.4) 461 (2.4) 779 (4.0) 1442 (7.4) 2142 (11.1) 3718 (19.2) 6309 (32.6) 4522 (23.3) 134 (0.69) 3787 (19.55) 522 (2.69) 11 (0.06) 4064 (20.95) 914 (4.72) 3150 (16.23) 296 (1.53) 776 (4.01) 6098 (31.48) 14366 (74.15) 389 (2.01) 4122 (21.28) 402 (2.08) 94 (0.48) Blacks, n (%) 5466 (22.0) 2367 (43.3) 3099 (56.7) 2204 (40.3) 977(41.3) 1227 (39.6) 440 (8.1) 689 (12.6) 861 (15.7) 866 (15.8) 1043 (19.1) 986 (18.1) 581 (10.6) 655 (11.98) 777 (14.22) 82 (1.50) 9 (0.16) 1675 (30.64) 485 (8.87) 1190 (21.77) 117 (2.14) 345 (6.31) 1371(25.08) 3319 (60.72) 604 (11.05) 1078 (19.72) 424 (7.76) 41 (0.75) ICU, intensive care unit; HIV, human immunodeficiency virus. RESULTS Among all patients with sepsis who were admitted to New Jersey acute care hospitals in 2002, we identified 19,373 whites and 5,466 blacks. Characteristics of these patients are shown in Table 1. Figure 1 shows the population-based, age-specific hospitalization rates for blacks and whites. The rates increased with age in both groups in an exponential fashion. We calculated the relative risk of hospitalization with sepsis in blacks vs. whites in different age groups. The results presented in Figure 2 indicate that the risk of sepsis in the black population is much greater than in the white population, especially in the younger age 764 Figure 1. Hospitalization rates in white and black patients with sepsis in different age groups. groups. The relative risk of sepsis in blacks compared with whites was greatest in patients 35– 44 yrs old (relative risk, 4.35; 95% confidence interval [CI], 3.93– 4.82) and then steadily decreased with age. However, it remained significant (relative risk, 1.72; 95% CI, 1.58 –1.87), even in the oldest age group ( 85 yrs old). The average age of white patients with sepsis was 72.8 0.11 yrs; black patients were significantly younger, 61.6 0.25 yrs (p .0001). Figure 3 displays the age distribution of hospitalized white and black patients with sepsis. Half of blacks with sepsis (52.2%) were 65 yrs old in contrast to a quarter of whites (24.9%). Table 2 shows age-adjusted rates of hospitalization, mortality, and hospital case fatality for black and white patients with sepsis, both men and women. Ageadjusted hospitalization and mortality rates for blacks were significantly greater Crit Care Med 2007 Vol. 35, No. 3 Figure 2. Relative risk of sepsis in blacks vs. whites in different age groups. I bars represent 95% confidence interval for relative risk. Figure 3. Age distribution of white and black patients with sepsis. Table 2. Age-adjusted rates of hospitalization, mortality, and hospital case fatality for white and black patients with sepsis Rates Race/Sex White Male Female Total Black Male Female Total a Hospitalizationa Mortalitya Case Fatalityb 426.8 332.6 371.6 885.4 814.2 846.4 4.52 3.37 2.69 19.78 14.82 11.82 119.7 86.2 99.6 219.5 200.9 208.6 2.41 1.65 1.37 10.39 7.48 6.04 27.17 25.44 26.15 26.48 25.78 25.88 0.55 0.49 0.36 1.41 0.99 0.79 Per 100,000 population; bper 100 sepsis hospitalizations. Data provided as mean SE. than for whites (p .0001). In whites, both these rates in men were significantly greater than in women. In blacks, only hospitalization rates were greater in men than in women. Crit Care Med 2007 Vol. 35, No. 3 Age-adjusted case fatality rates, however, were similar for whites and blacks of both sexes. We also did not find differences in case fatality rates between whites and blacks in various age groups. How- ever, like hospitalization rates, case fatality rates for sepsis increased significantly with age, both in whites (p .0001) and blacks (p .0001). Black patients with sepsis were more likely than white patients to be admitted to the hospital from the emergency room (odds ratio [OR], 1.4; 95% CI, 1.27–1.50) and to the intensive care unit (OR, 1.14; 95% CI, 1.07–1.21). Both the hospital and intensive care unit lengths of stay were greater for blacks than for whites (17.9 0.26 days vs. 15.2 0.12 days, p .0001, and 4.3 0.14 days vs. 3.7 0.07 days, p .0002, respectively). Hospitalized blacks were 3.28 times more likely to be uninsured compared with whites (95% CI, 3.22–3.34). Among patients with sepsis, this difference was even greater (OR, 3.96; 95% CI, 3.44 – 4.56). We compared the frequency of some sepsis-related co-morbidities in blacks vs. whites. The difference in the frequency of the accompanying HIV infection between blacks and whites was significant in all age groups (Fig. 4). Overall, the likelihood of having HIV infection in black patients with sepsis compared with whites was 19.6 times greater (95% CI, 16.19 –23.60). Among patients with sepsis, black patients were more likely than white patients to have diabetes (OR, 1.97; 95% CI, 1.75–2.20 for diabetes type I and OR, 1.43; 95% CI, 1.33–1.54 for diabetes type II), obesity (OR, 1.41; 95% CI, 1.14 – 1.75), burns (OR, 2.90; 95% CI, 1.20 –7.01), and chronic renal failure (OR, 1.61; 95% CI, 1.42–1.84) but were less likely to have cancer (OR, 0.68; 95% CI, 0.63– 0.74), trauma (OR, 0.55; 95% CI, 0.43– 0.69), and urinary tract infection (OR, 0.73; 95% CI, 0.68 – 0.78). We also calculated these values for hospitalized patients who did not have sepsis and found the same associations. However, the likelihood of having HIV infection (OR, 14.2; 95% CI, 13.53–14.95), diabetes type II (OR, 1.30; 95% CI, 1.28 – 1.32), and cancer (OR, 0.59; 95% CI, 0.58 – 0.60) in blacks compared with whites among nonseptic patients was significantly smaller than in patients with sepsis. The odds ratios in nonseptic hospitalized blacks vs. whites for diabetes type I (OR, 1.77; 95% CI, 1.72–1.82), obesity (OR, 1.41; 95% CI, 1.37–1.44), trauma (OR, 0.68; 95% CI, 0.66 – 0.70), burns (OR, 1.39; 95% CI, 1.15– 1.68), and chronic renal failure (OR, 1.68; 95% CI, 1.60 –1.76) were similar to those in patients with sepsis. In addition, the odds ratio of having urinary tract infection in black vs. white patients without sepsis was 765 Figure 4. Proportion of persons with human immunodeficiency virus infection among white and black patients with sepsis in different age groups. even greater than in the septic group (OR, 0.86; 95% CI, 0.84 – 0.89). Because of the extraordinarily high value of the odds ratio for having HIV infection in blacks vs. whites in comparison with the other co-morbidities, we analyzed the association between race and sepsis onset in hospitalized black and white patients with and without HIV infection. Among HIV patients, blacks were 1.60 times more likely to have sepsis than whites (95% CI, 1.32–1.94). Among hospitalized patients without HIV, blacks compared with whites were 1.16 times more likely to have sepsis (95% CI, 1.13–1.20). Although the odds ratio of having sepsis in blacks vs. whites among patients with HIV was significantly greater than in patients without HIV, the latter was still significant. DISCUSSION We found that the rates of hospitalization and mortality for sepsis in blacks were greater than in whites, without differences in rates of case fatality. We also found that blacks with sepsis were younger, more likely to have HIV, diabetes, chronic renal failure, burns, and to be obese than whites. In contrast, whites with sepsis were older and were more likely to have cancer and trauma. However, only the odds ratios for HIV, diabetes type II, and cancer seemed to distinguish septic from nonseptic hospitalized patients. Our results confirm findings from earlier studies showing that the rates of hospitalization and mortality for sepsis are higher among blacks than in whites (3, 5, 766 7–11, 13). However, this study examines the possible reasons for these greater rates of sepsis hospitalization in black patients compared with whites. For our analysis, we used the 2002 New Jersey State Inpatient Database developed as part of the Healthcare Cost and Utilization Project. In contrast to the national databases that usually have under representation of race data (up to 30% missing race data), this state database has only 2.5% missing race data. Vascular diseases, cancer, diabetes, trauma, and HIV/AIDS account for most of the reported differences in health status between blacks and whites (14 –18). In addition, Wong et al. (16) reported that infections contributed to 21% of disparity in mortality from any cause, second only to cardiovascular disease. Among all infections, HIV infection has been found to be the most important cause of disparity in life expectancy between blacks and whites. Similarly, we found that hospitalized blacks were many times more likely to have HIV infection than whites, and what was striking was the fact that among persons with sepsis, this difference was even greater. Thus, the greater prevalence of HIV infection in the black population compared with the white population may be one of the most important reasons for the increased sepsis hospitalization rates and, correspondingly, population-based sepsis mortality rates in blacks. Increasing age is a significant risk factor for sepsis (4, 19, 20). However, we found that black patients with sepsis were considerably younger than whites. In the population 65 yrs of age, a substantial number of persons are uninsured and experience difficulties accessing health care due to cost or medical bill problems (21). The proportion of uninsured persons among blacks is greater than among whites. In 2002, among New Jersey residents 65 yrs of age, 20.7% of blacks were uninsured compared with 11.3% of whites (22). Furthermore, the poverty rate in blacks in New Jersey (29%) is 3.6 times greater than in whites (8%) (23). Thus, black patients might experience difficulties accessing timely and highquality health care in the initial stage of any infectious process, delaying timely treatment, which might prevent the onset of sepsis. These sociodemographic factors may also explain the greater proportion of black patients with sepsis admitted through the emergency room and to the intensive care unit. On the other hand, it has been shown that racial disparities in health status depend not only on sociodemographic differences (24 –26) but on other factors as well. Some chronic underlying medical conditions and medical procedures significantly increase the risk of sepsis onset. Patients with immune deficiency, malignancy, and diabetes mellitus are particularly susceptible to bacterial infection and subsequent sepsis (4, 27–34). The increased rates of diabetes mellitus in blacks compared with whites may be another important predisposing factor for the racial disparities in sepsis. Indeed, the odds ratio for diabetes type II in black vs. white patients was higher in septic patients than in nonseptic patients. Danai et al. (35) found a greater risk for sepsis in blacks with cancer than in whites. Black patients with sepsis in our study had a smaller likelihood of having cancer compared with white patients. This might be explained by the fact that cancer incidence increases with increasing age, and black patients in our study group were significantly younger than white patients and therefore less likely to have cancer. Septicemia was one of the ten leading causes of death for blacks in the United States in 2002, but it was not among the top ten causes of death for whites (36). Despite the greater rate of populationbased sepsis mortality in blacks compared with whites in our study, case fatality rates in white and black patients with sepsis were similar. Williams et al. (37) also did not find racial differences in the hospital survival of patients admitted to the Crit Care Med 2007 Vol. 35, No. 3 intensive care unit. These similar rates of case fatality do not suggest systematic differences in the treatment of sepsis between blacks and whites or suggest that any that do exist are inconsequential with respect to in-hospital mortality. The limitations of this study are commonly associated with the use of the administrative hospital discharge data (38). In 2002, there was no specific code for sepsis in the ICD-9-CM, and we used codes for septicemia to select patients with sepsis. This method was previously validated by Martin et al. (3) in analyzing an administrative database. New ICD9-CM codes 995.91 (“Systemic inflammatory response syndrome due to infectious process without organ dysfunction,” which is sepsis) and 995.92 (“Systemic inflammatory response syndrome due to infectious process with organ dysfunction,” which is severe sepsis) became effective October 1, 2002. However, we found that in our database, the ICD-9-CM codes 995.91 and 995.92 were registered only in 0.06% and 0.17% of hospital discharges with septicemia, respectively. Moreover, according to the instructions, these codes must accompany a code from the category 038 (septicemia). We assume some misclassification due to the inaccuracies in diagnostic coding. A small number of records with missing information on race (2.3% among discharges with sepsis) might inconsiderably affect the results obtained. Our results are based on the secondary analysis of the publicly available administrative data that contain hospital inpatient discharge records in the State of New Jersey. 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