Epidemiology of Hospital‐Acquired Infections in Veterans With Spinal Cord Injury and Disorder
Objective. To describe the epidemiology of hospital‐acquired infections (HAIs) in veterans with spinal cord injury and disorder (SCI&D).
Design. Retrospective medical record review.
Setting. Midwestern Department of Veterans Affairs spinal cord injury center.
Participants. A total of 226 patients with SCI&D hospitalized at least once during a 2‐year period (October 1, 2001, through September 30, 2003).
Results. A total of 549 hospitalizations were included in the analysis (mean duration of hospitalization, 33.7 days); an HAI occurred during 182 (33.2%) of these hospitalizations. A total of 657 HAIs occurred during 18,517 patient‐days in the hospital (incidence rate, 35.5 HAIs per 1,000 patient‐days). Almost half of the 226 patients had at least 1 HAI; the mean number of HAIs among these patients was 6.0 HAIs per patient. The most common HAIs were urinary tract infection (164 [25.0%] of the 657 HAIs; incidence rate, 8.9 cases per 1,000 patient‐days), bloodstream infection (111 [16.9%]; incidence rate, 6.0 cases per 1,000 patient‐days), and bone and joint infection (103 [15.7%]; incidence rate, 5.6 cases per 1,000 patient‐days). The most common culture isolates were gram‐positive bacteria (1,082 [45.6%] of 2,307 isolates), including Staphylococcus aureus, and gram‐negative bacteria (1,033 [43.6%] of isolates), including Pseudomonas aeruginosa. Multivariable regression demonstrated that predictors of HAI were longer length of hospital stay (P = .002), community‐acquired infection (P = .007), and use of a urinary invasive device (P = .01) or respiratory invasive device (P = .04).
Conclusions. The overall incidence of HAIs in persons with SCI&D was higher than that reported for other populations, confirming the increased risk of HAI in persons with spinal cord injury. The increased risk associated with longer length of stay and with community‐acquired infection suggests that strategies are needed to reduce the duration of hospitalization and to effectively treat community‐acquired infection, to decrease infection rates. There is significant room for improvement in reducing the incidence of HAIs in this population.
Received July 27, 2007; accepted October 24, 2007; electronically published February 4, 2008.
Approximately 253,000 persons are living with spinal cord injury (SCI) in the United States, with an annual incidence of 11,000 new cases each year.1 Use of the healthcare system is high during the lifetime of a person with a SCI, resulting in high costs to both individuals and the healthcare system. The average yearly cost after the first year of injury ranges from $27,568, for those with paraplegia, to $132,807, for those with tetraplegia, and lifetime costs for a 50‐year‐old person with SCI approaching $1.7 million.1 Hospital‐acquired infection (HAI) is a common complication in persons with spinal cord injury and disorder (SCI&D), whether it occurs during initial hospitalization after injury or during subsequent hospitalizations for long‐term care of injuries and other problems. Frequent and often prolonged hospitalizations in this population also increase the risk of acquiring antibiotic‐resistant microorganisms.2
Infections are a leading cause of death for persons with SCI&D; pneumonia and septicemia causing most infection‐related deaths (approximately 35%).3,4 In the general population, HAIs are associated with increased length of stay (LOS) in the hospital, increased cost, and increased mortality.5 Recent data have shown that HAIs may have long‐term effects, increasing the number of hospitalizations and the LOS in veterans with SCI.6 Risk factors for HAIs are well established in the general population; they include underlying health impairment, an increased number of comorbidities, urinary catheterization, surgery, presence of foreign bodies, and certain respiratory procedures.5,7‐10 There is also an increasing incidence of infections previously considered community‐acquired, such as infection with community‐associated methicillin‐resistant Staphylococcus aureus (MRSA), in hospitalized patients.11
Mylotte et al.12 showed that persons with SCI undergoing short‐term rehabilitation were at an increased risk of HAI, compared with persons without SCI undergoing short‐term rehabilitation. HAIs were identified in 25.8% of admitted patients with SCI undergoing short‐term rehabilitation, compared with 16.6% in admitted patients without SCIs (P = .001). The incidence of HAIs was 6.72 episodes per 1,000 patient care–days in the SCI group and 5.48 episodes per 1,000 patient care–days in the non‐SCI group. The most common infections in persons with SCI were urinary tract infection, bloodstream infection, and surgical wound infection. The mean time to development of an HAI was 15 days.12
The literature on HAIs in persons with SCI is limited and has focused primarily on the short‐term rehabilitation phase of treatment. The Healthy People 201013 objectives for persons with disabilities, which include persons with SCI&D, address the disparities in research findings and the need for collection of data on assessment of secondary conditions in this population. We hypothesized that the literature would show that the incidence of HAI in this population would be high compared with that in the general population, and that the most common HAIs would be urinary tract infection, blood stream infection, and respiratory tract infection. The purpose of this study was to describe the epidemiology of HAIs in veterans with SCI&D, subsequent to the initial injury rehabilitation period.
Methods
Study Design
We performed a retrospective review of the medical records of veterans with SCI&D who were admitted at least once to a Midwestern Veterans Affairs SCI center during the 2‐year period from October 1, 2001 through September 30, 2003. Patients with SCI&D were defined as those with a diagnosis of traumatic or nontraumatic lesions of the spinal cord.
HAI Definition
An HAI was defined as any infection that was identified 48 hours or more after admission to the hospital with no evidence of incubating infection at the time of admission. Definitions were based on the Centers for Disease Control and Prevention (CDC) National Nosocomial Infections Surveillance system criteria for identification of specific types of HAIs.14,15 Specifically, HAI definitions were based on algorithms that combined specific clinical findings with results of laboratory tests and other diagnostic tests. Clinical findings were extracted through review of the information in the patient medical record. Laboratory results collected included microbiology data, chemistry and hematology data, and imaging and radiology data. Expert clinicians refined and clarified infection identification, definitions, and other uncertainties found in the patient data. For example, because many people with SCI&D use some type of urinary invasive device, colonization of the urinary tract with bacteria is common. Therefore, the definition of a clinically important urinary tract infection in patients with SCI&D includes the presence of bacteriuria, evidence of tissue invasion (pyuria), and clinical symptoms. Community‐acquired infection was defined as any infection determined to be incubating at the time of admission or detected by a positive result of a microbiology culture of a sample obtained within 48 hours after admission.
Data Sources and Covariates
The patient medical record was used to identify HAI or community‐acquired infection, type of microorganisms isolated, demographic characteristics, hospital LOS, in‐hospital mortality, number and type of invasive devices used, and antibiotic exposure in the 30 days before admission. Demographic data collected were sex, ethnicity, age, and marital status. The types of invasive devices assessed were urinary catheters (indwelling, suprapubic, intermittent, external, and urinary diversion), respiratory invasive devices (ventilators, endotracheal tube, and others used for tracheostomy), gastrointestinal invasive devices (gastrostomy tube or jejunostomy tube), and intravascular catheters (peripheral or intravascular catheter lines, arterial lines, peripherally inserted central catheter lines, infusion ports, and Hickman catheters).
The Veterans Affairs Spinal Cord Dysfunction Registry was used to obtain data on level of injury, completeness of injury, age at onset, and duration of injury. Information was missing for approximately 10% of the sample subjects for any particular SCI characteristic variable. To avoid losing subjects in the sample, a missing dummy category was made for each SCI characteristic variable so that those subjects with missing data could be incorporated into the multivariable model.
The Veterans Affairs Medical Inpatient and Outpatient data sets were used to obtain information on comorbidities, receipt of home health care in the previous 30 days, admission from a nursing home, and in‐hospital mortality. Comorbidities were identified by presence of International Classification of Diseases, Ninth Revision, Clinical Modification codes in medical record for the year before the infection or during the same hospitalization as the infection occurred. The following comorbid disease and conditions were selected: myocardial disease (includes myocardial infarction and congestive heart failure), vascular disease (includes peripheral vascular disease and cerebrovascular disease), dementia, chronic obstructive pulmonary disease, liver disease, diabetes (including diabetes with end‐organ damage), cancer (including hematologic and solid tumor neoplasms), and AIDS. These comorbid conditions were selected based on the Deyo‐Charlson Comorbidity index, although this index was not used for this study.16
Statistical Analysis
The incidence rate of HAI was calculated as the number of cases of HAI divided by the total number of hospital‐days during the 2‐year study period. This incidence rate was also calculated according to site of infection. The proportion of patients with HAI was calculated as the number of patients with any HAI divided by the total number of patients with at least 1 hospitalization during the 2‐year study period. The mean number of infections per patient was calculated as the total number of infections divided by the total number of patients with at least 1 infection.
For unadjusted analyses, categorical demographic, injury, and medical characteristics were assessed by infection status using χ2 tests. The 2‐sample Student t test was used to assess any differences in continuous variables and risk of an infection. For the unadjusted analyses, the unit of analysis was the patient and the hospitalization. Multivariable logistic regression analyses using generalized estimating equations were used to identify factors predictive of HAI. The final model included variables that were significant and/or modified the odds ratios of any other variable by more than 10%. Variables that did not fit these criteria were dropped from the model. For the multivariable logistic regression model, the unit of analysis was the hospitalization.
Prolonged LOS in the hospital is associated with increased risk of developing infection; however, development of infection during hospitalization is also associated with prolonged LOS. This reverse causality (endogeneity bias) can result in a correlation between the error terms and the independent variables, which in turn results in biased estimates.17 Because methods of addressing this bias in the analysis of a continuous exposure and a dichotomous outcome are not clear, we constructed a multivariable negative binomial model to predict LOS in this sample. The predicted LOS was then used as the independent variable in the multivariable logistic regression model to identify factors that predict development of an HAI. Use of the values for predicted LOS (which are presented in the article) did not significantly modify the findings obtained with use of the values for actual LOS, but it increased the standard errors, with the result that some factors became nonsignificant at the .05 level.
Age, duration of injury, and age at onset of SCI&D were correlated on the basis of Pearson correlation statistics. Age and duration of injury were both included in the final model since they did not change the results significantly in their individual models. In addition, since there were so few women in the study, sex was not included as a predictor in the final model. The final model was also repeated including only survivors of the hospitalizations. All analyses were conducted using SAS software version 8.2 (SAS).
Results
Two hundred twenty‐six patients with SCI&D had at least 1 hospitalization during the 2‐year study period. Nearly all patients were male (224 [98%]), and the ethnicity distribution was as follows: non‐Hispanic white, 126 (56%); African American, 75 (33%); Hispanic, 7 (3%); and unknown, 18 (8%). The mean age of the patients was 58.3 years. The mean age at injury onset was 37.0 years, and the mean duration of injury was 20.9 years. There were almost equal numbers of patients with tetraplegia (113 [50%]) and paraplegia (103 [46%]); for 10 (4%) of patients, the level of injury was unknown.
There were a total of 549 hospitalizations (an HAI occurred in 182 [33.2%]), with a mean patient LOS of 33.7 days (median, 14.0 days). The mean LOS for hospitalizations in which the patient developed an HAI was significantly longer than that for hospitalizations in which the patient did not develop an HAI (64.3 vs. 18.6 days; 
). The mean time from admission to the onset of the first HAI was 15.0 days (median, 8.0 days; range, 3‐105 days). A total of 22 (9.7%) of the 226 patients died during hospitalization; 15 (13.6%) of the 110 with an HAI died and 7 (6.0%) of the 116 without an HAI died (
).
During 18,517 patient‐days in the hospital for 226 patients, 657 HAIs were identified. The incidence rate was 35.5 HAIs per 1,000 patient‐days. Of the 226 patients with at least 1 hospitalization, 110 (48.7%) had at least 1 HAI. Among the 182 hospitalizations in which an HAI occurred, there were 3.6 HAIs per hospitalization. Five hundred sixty‐two (86%) of the 657 HAIs occurred in the SCI unit, 38 (5.8%) occurred in the medical intensive care unit, and the other 57 (8.2%) occurred in other units.
The most frequent HAIs in veterans with SCI&D were urinary tract infection (164 [25.0%] of the 657 HAIs), blood stream infection (111 [16.9%]), and bone and joint infection (103 [15.7%]). The incidence rates for all sites (expressed in HAIs per 1,000 patient‐days) are given in Table 1; the incidence rate for each type of infection ranged from 0.2 to 8.9 HAIs per 1,000 patient‐days.
Classes of microorganisms that colonized or infected patients included gram‐positive bacteria (1,082 [45.6%] of 2,370 isolates), gram‐negative bacteria (1,033 [43.6%]), fungi (210 [8.9%]), and other organisms (45 [1.9%]). The most common isolates recovered from patients with HAIs were Staphylococcus aureus (348 [14.7%] of 2,370 isolates; 321 [92.2%] of those 348 were MRSA), other Staphylococcus species (255 [10.8%]), Pseudomonas aeruginosa (267 [11.3%]), untyped gram‐negative bacilli (257 [10.8%]), and Candida species (210 [8.9%]) (Table 2). The most frequently recovered isolates for the 3 most common HAIs were as follows: for urinary tract infection (n = 613 isolates), P. aeruginosa (76 isolates [12.4%]), Enterococcus faecium (63 [10.3%]), untyped gram‐negative bacilli (61 [10.0%]), and S. aureus (57 [9.3%]); for bloodstream infection (n = 509 isolates), S. aureus (96 isolates [18.9%]), other Staphylococcus species (72 [14.2%]), and untyped gram‐negative bacilli (54 [10.6%]); for bone and joint infection (n = 314 isolates), S. aureus (48 isolates [15.3%]), untyped gram‐negative bacilli (40 [12.7%]), and P. aeruginosa (34 [10.8%]).
Table 3 describes the demographic characteristics associated with occurrence of an HAI. Persons with SCI&D who had at least 1 occurrence of an HAI were older than those without an HAI (mean age, 60.4 years vs. 56.3 years; P = .03). Unknown level of injury, longer duration of injury, and greater age at onset of SCI was associated with no occurrence of an HAI. No significant differences were found between sex and ethnicity and HAI status.
In 195 (35.5%) of the 549 hospitalizations, the patient had a community‐acquired infection at admission; in 62 hospitalizations [11.3%], the patient had been admitted from a nursing home; and in 200 hospitalizations [36.4%], the patient had received home health care in the 30 days before admission. For more than two‐thirds of hospitalizations (362 [65.9%]), the patient had received antibiotics in the 30 days before admission. For more than half of the hospitalizations (323 [58.8%]), the patient had at least 1 comorbid illness reported; the mean number of patient comorbidities per hospitalization was 1.1 (mean number per patient, 0.7).
Table 4 indicates that presence of an infection at admission (ie, community‐acquired infection), receipt of home care in the 30 days before admission, antibiotic exposure in the previous 30 days, presence of 1 or more comorbidities, and use of a invasive device during the hospitalization were significantly associated with occurrence of an HAI. Admission from a nursing home was not significantly associated with occurrence of an HAI.
Dementia was the only comorbid condition associated with occurrence of an HAI (P = .003) (Table 4). Although the patient had diabetes or chronic obstructive pulmonary disease in one‐quarter of hospitalizations, these diseases were not associated with infection.
In 177 (97.3%) of the 182 hospitalizations in which an HAI occurred, the patient had some type of invasive device used during the hospitalization. Use of specific types of devices also were associated with infection status (Table 4). Patients with HAIs were more likely to have used a urinary device (P < .0001), an intravascular device (P = .0002), a gastrointestinal device (P < .0001), or a respiratory device (P = .005) than were patients without infection.
Table 5 describes multivariable regression results for assessment of patient characteristics independently associated with occurrence of an HAI during hospitalization. Longer LOS was significantly associated with occurrence of an HAI (P = .002): for each additional day in the hospital, the predicted LOS increased the risk of HAI by 2%. Similar to the bivariable analysis, the multivariable analysis showed that admission with a community‐acquired infection (OR, 1.82 [95% confidence interval (CI), 1.17‐2.82]; P = .007) and use of a urinary device (OR, 3.24 [95% CI, 1.29‐8.12]; P = .01) or respiratory device (OR, 2.16 [95% CI, 1.05‐4.45]; P = .04) were significantly associated with occurrence of an HAI during hospitalization. After adjustment for other variables in the model, we found that demographic and injury characteristics, receipt of home health care, previous antibiotic exposure, and use of a intravascular or gastrointestinal device were not associated with occurrence of HAI during hospitalization. Results were similar in a model that included only hospitalizations in which the patient survived (data not presented).
Discussion
The purpose of this research was to characterize the types and magnitude of HAIs in veterans with SCI&D. This information will help clinicians and healthcare administrators evaluate current management and infection control practices and aid in identifying modifiable practices to reduce HAIs in this population. A recent review of HAI surveillance and control policies found that 30% or more of HAIs are preventable.18 The adverse outcomes that often result from HAIs, including morbidity and death, underscore the need to reduce the incidence of HAIs in persons with SCI.19 The cost benefit of reducing the incidence of these infections could be substantial. Not only could the direct costs of treating the infection be reduced (eg, antibiotics), but also the subsequent costs due to morbidity (eg, cost of increased LOS and provider time) and untimely deaths would be reduced.
Our first hypothesis was supported by the results that indicate that the overall incidence of HAIs in this population (35.5 HAIs per 1,000 patient‐days) was higher than what has been reported in the literature for persons with SCI&D (range, 6.7‐13 HAIs per 1,000 patient‐days).12,20 This finding is likely due to this study’s focus on patients with chronic SCI&D, as opposed to other studies that have focused on short‐term rehabilitation patients. The overall incidence found in this study was also much higher than that in other patient populations (range, 2.2‐15.0 cases per 1,000 patient‐days),9,21,22 which supports the hypothesis that presence of an SCI puts the patient at increased risk for developing an HAI. The results may also be the result of the long LOS for persons with SCI&D, compared with that for other populations. Increased LOS is associated with significantly increased risk of infection.10
Impaired immune and inflammatory response may also be an important factor in the increased risk of HAI in persons with SCI&D. Suppression of immune function in persons with SCI&D has been linked to impairment in the neurologic systems that influences the inflammatory and immune response.23,24 In addition, barrier defense can be impaired because of the frequent use of invasive devices and/or skin breakdown that results in pressure ulcers. These problems can result in chronic inflammation and erosive changes in the mucosa of the bladder, lung, or other sites, reducing the effects of mucosal enzymes that usually prevent bacterial adherence.24 Patients who have intact bladder and bowel function and have protective sensation and greater mobility are less likely to get HAIs. Cases of SCI&D in which level and duration of injury were unknown (because of missing data) are suspected, on the basis of clinical experience, to be more common among patients who do not have a clear level of injury to document because they either have a less severe SCI or a different cause of the SCI, such as cervical spondylotic myelopathy. These patients often have fewer ports of entry for infection and are likely to spend less time in the hospital.
Urinary tract infections and blood stream infections are 2 of the most common HAIs found in the general population and likewise were the 2 most common HAIs found in this study of persons with SCI&D. Contrary to our second hypothesis, which was that respiratory tract infections would be among the 3 most common HAIs, we found that bone and joint infections were the third most common HAIs. Although these infections, including osteomyelitis and osteomyelitis associated with a pressure ulcer, are prevalent problems in persons with SCI,25 the number of infections we found was higher than expected. The isolates most commonly associated with bone and joint infections in persons with SCI&D were similar to those reported in the literature: S. aureus, P. aeruginosa, and other gram‐negative bacilli.25,26
The microorganisms isolated in culture in our study are similar to those found in other studies of SCI populations and the general population.12 The high prevalence of MRSA in this population suggests interventions are needed to reduce the rates of colonization, infection, and transmission of this organism. Common organisms in urinary tract infections included enterococci, untyped gram‐negative bacilli, and S. aureus. It is likely that the high incidence of staphylococcal urinary tract infection reflects the frequent use of urinary catheterization in persons with SCI&D.27 Escherichia coli is often associated with urinary tract infection25,28,29 and accounted for 7.4% of isolates in this study. The most common pathogens in blood stream infections are S. aureus, coagulase‐negative staphylococci, aerobic gram‐negative bacilli, Candida species, and enterococci,30 which was consistent with the findings of this study. S. aureus was the organism most commonly isolated from bone and joint infections in our study, which is consistent with the literature.26 Gram‐negative bacilli were also common.
Greater hospital LOS was strongly associated with occurrence of an HAI in our study, even after using the predicted LOS to account for endogeneity. This finding may explain why the mean time to onset of infection was almost 2 months. Receipt of home health care and antibiotic exposure were not independent predictors of HAI after adjustment for other covariates, but presence of a community‐acquired infection remained an important predictor of HAI. This is not surprising, since there has been a trend of common community‐acquired organisms showing up in hospitals.11 In addition, patients infected in the community could remain colonized in other anatomic areas after antibiotic treatment, resulting in a source for future HAI.
Most patients used some type of invasive device, and use of urinary and respiratory invasive devices was associated with infection, after adjustment for other factors. The CDC National Nosocomial Infections Surveillance system data and other studies have shown increased rates of HAI associated with specific types of invasive devices.5,31,32
Further analyses of specific infections may have identified other factors associated with these HAIs; however, the size of the sample precluded this type of analysis. Another limitation of this study was that it focused on a single facility; thus, its generalizability to other populations of patients with SCI&D is limited. Since this study assessed association and not causality, the increased LOS associated with occurrence of an HAI may actually be the result of infection, particularly since half of the first infections occurred within the first 8 days after admission, although use of the predicted LOS was intended to account for endogeneity.
These results indicate that there is significant room for improvement in preventing HAIs in persons with SCI&D. One of the goals of the CDC and Healthy People 2010 objectives is to reduce disparities in outcomes among persons with disabilities. This study highlighted the high risk of HAI for persons with SCI&D. The HAI rate was high, which emphasizes the potential impaired immune response that persons with SCI&D may have, particularly with respect to urinary tract infections, blood stream infections, and bone and joint infections. Longer LOS, presence of a community‐acquired infection, and use of invasive devices were factors associated with HAI in this study population. Thus, prevention of HAI in this population may be possible by decreasing the number of hospitalizations, identifying and treating community‐acquired infections quickly and appropriately, and minimizing the rate of use and the duration of use of invasive devices. Future research should focus on efforts to decrease the incidence of HAIs in this patient population and address barriers and facilitators to implementing these interventions and to monitor outcomes.
Acknowledgments
Financial support. This material is based on work supported by the Department of Veterans Affairs, Office of Research and Development, Health Services Research and Development Service (LIP 42‐074).
Disclaimer. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the Department of Veterans Affairs.
Potential conflict of interest. Dr. Parada is a speaker for Pfizer. All other authors report no potential conflicts of interest relevant to this article.
References
- 1. National SCI Statistical Center. Spinal Cord Injury Facts and Figures at a Glance. June 2006. National Institute on Disability and Rehabilitation Research, Washington, DC. Available at: http://www.spinalcord.uab.edu. Accessed October 11, 2007.
- 2. Montgomerie JZ. Infections in patients with spinal cord injuries. Clin Infect Dis 1997; 25:1285‐1290.
- 3. DeVivo M, Stover S. Long term survival and causes of death. In: Stover SL, DeLisa JA, Whiteneck GG, eds. Spinal Cord Injury Clinical Outcomes From the Model Systems. Gaithersburg, MD: Aspen Publishers; 1995:289‐313.
- 4. DeVivo MJ, Krause JS, Lammertse DP. Recent trends in mortality and causes of death among persons with spinal cord injury. Arch Phys Med Rehabil 1999; 80:1411‐1419.
- 5. Vincent J. Nosocomial infections in adult intensive‐care units. Lancet 2003; 361:2068‐2077.
- 6. LaVela SL, Evans CT, Miskevics S, Parada JP, Priebe M, Weaver FM. Long‐term outcomes from nosocomial infections in persons with spinal cord injuries and disorders. Am J Infect Control 2007; 35:393‐400.
- 7. Pittet D, Theivent B, Wenzel RP, Li N, Gurman G, Suter PM. Importance of pre‐existing co‐morbidities for prognosis of septicemia in critically ill patients. Intensive Care Med 1993; 19:265‐272.
- 8. Gross PA, DeMauro, van Antwerpen C, Wallenstein S, Chiang S. Number of comorbidities as a predictor of nosocomial infection acquisition. Infect Control Hosp Epidemiol 1988; 9:497‐500.
- 9. Richards MJ, Edwards JR, Culver DH, Gaynes RP. Nosocomial infections in combined medical‐surgical intensive care units in the United States. Infect Control Hosp Epidemiol 2000; 21:510‐515.
- 10. Chotani RA, Roghmann M, Perl TM. Nosocomial infections. In: Nelson KE, Williams CM, Graham NMH, eds. Infectious Disease Epidemiology: Theory and Practice. Gaithersburg, MD: Aspen Publishers; 2001:357‐407.
- 11. McGowan JE. The impact of changing pathogens of serious infections in hospitalized patients. Clin Infect Dis 2000;31(suppl 4):S124‐S130.
- 12. Mylotte JM, Graham R, Kahler L, Young L, Goodnough S. Epidemiology of nosocomial infection and resistant organisms in patients admitted for the first time to an acute rehabilitation unit. Clin Infect Dis 2000; 30:425‐432.
- 13. US Department of Health and Human Services. Healthy People 2010 with Understanding and Improving Health and Objectives for Improving Health. 2 vols. 2nd ed. Washington, DC: US Government Printing Office; 2000.
- 14. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections. Am J Infect Control 1988; 16:128‐40.
- 15. Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TC. CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections. Infect Control Hosp Epidemiol 1992; 13:606‐608.
- 16. Deyo RA, Cherkin DC, Ciol MA. Adapting a clinical comorbidity index for use with ICD‐9‐CM administrative databases. J Clin Epidemiol 1992; 45:613‐619.
- 17. Graves N, Weinhold D, Tong E, et al. Effect of healthcare‐acquired infection on length of hospital stay and cost. Infect Control Hosp Epidemiol 2007; 28:280‐292.
- 18. Gastmeier P. Nosocomial infection surveillance and control policies. Curr Opin Infect Dis 2004; 17:295‐301.
- 19. Chen Y, Chou Y, Chou P. Impact of nosocomial infection on cost of illness and length of stay in intensive care units. Infect Control Hosp Epidemiol 2005; 26:281‐287.
- 20. Nicolle LE, Buffet L, Alfien N, Tate R. Nosocomial infections on a rehabilitation unit in an acute care hospital. Infect Control Hosp Epidemiol 1988; 9:553‐558.
- 21. Josephson A, Karanfil L, Alonso H, Watson A, Blight J. Risk‐specific nosocomial infection rates. Am J Med 1991;91(suppl 3b):131S‐137S.
- 22. Urrea M, Pons M, Serra M, Latorre C, Palomeque A. Prospective incidence study of nosocomial infections in a pediatric intensive care unit. Pediatr Infect Dis J 2003; 22:490‐494.
- 23. Nash MS. Known and plausible modulators of depressed immune functions following spinal cord injuries. J Spinal Cord Med 2000; 23:111‐120.
- 24. Frost FS, Pien LC. The immune system and inflammatory response in persons with SCI. In: Lin VW, Cardenas DD, Cutter NC, et al., eds. Spinal Cord Medicine: Principles and Practice. New York, NY: Demos Medical Publishing Inc; 2003:213‐220.
- 25. Darouiche RO. Infection and spinal cord injury. In: Lin VW, Cardenas DD, Cutter NC, et al., eds. Spinal Cord Medicine: Principles and Practice. New York, NY: Demos Medical Publishing Inc; 2003:201‐207.
- 26. Lew DP, Waldvogel FA. Osteomyelitis. Lancet 2004; 364:369‐379.
- 27. Ronald A. The etiology of urinary tract infection: traditional and emerging pathogens. Am J Med 2002; 113:14S‐19S.
- 28. Bennett CJ, Young MN, Darrington H. Differences in urinary tract infections in male and female spinal cord injury patients on intermittent catheterization. Paraplegia 1995; 33:69‐72.
- 29. Hamamci N, Dursun E, Akbas E, Aktepe OC, Cake A. A quantitative study of genital skin flora and urinary colonization in spinal cord injured patients. Spinal Cord 1998; 36:617‐620.
- 30. Banerjee SN, Emori TG, Culver DH, et al. Secular trends in nosocomial primary bloodstream infections in the United States, 1980‐1989. National Nosocomial Infections Surveillance System. Am J Med 1991; 91:86S‐89S.
- 31. Pien EC, Hume KE, Pien FD. Gastrostomy tube infections in a community hospital. Am J Infect Control 1996; 24:353‐358.
- 32. Centers for Disease Control and Prevention. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004; 32:470‐485.
-
Presented in part: 16th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America; Chicago, Illinois; March 18‐21, 2006 (abstract 211).