| | Elevated C-Reactive Protein Associated With Decreased High-Density Lipoprotein Cholesterol in Men With Spinal Cord InjuryAbstract Liang H, Mojtahedi MC, Chen D, Braunschweig CL. Elevated C-reactive protein associated with decreased high-density lipoprotein cholesterol in men with spinal cord injury. ObjectivesTo determine if people with spinal cord injury (SCI) have elevated C-reactive protein (CRP), to examine the association of CRP with high-density lipoprotein cholesterol (HDL-C), and to assess the influence of completeness and level of injury on these parameters. ParticipantsMen with SCI (n=129) who were free of infection and/or recent anti-inflammatory medication use as well as their 1:1 age- and race-matched able-bodied counterparts from the 1999–2002 National Health and Nutrition Examination Surveys. InterventionsNot applicable. Main Outcome MeasuresHigh CRP was defined as 3mg/L or higher and low HDL-C as less than 1.04mmol/L. ResultsMen with SCI were more likely to have high CRP (odds ratio [OR]=2.29; 95% confidence interval [CI], 1.33–3.95) and low HDL-C (OR=1.81; 95% CI, 1.01–3.27). The OR for low HDL-C in SCI was no longer significant when high CRP was controlled. CRP was higher in complete versus incomplete injury (median, 3.7mg/L vs 1.2mg/L; P=.005), and this elevation was independent of age, smoking, physical activity, waist circumference, and weight. No conclusion can be made on the association of injury level and CRP because of a lack of power. ConclusionsThe elevated CRP, possibly the major risk factor, together with decreased HDL-C may contribute to greater incidence for cardiovascular disease in the SCI population. MORBIDITY AND MORTALITY from cardiovascular disease (CVD) is greater among spinal cord–injured compared with able-bodied populations.1, 2, 3, 4 It was recently found that adult men with a spinal cord injury (SCI) had better metabolic profiles for all traditional risk factors for CVD, except high-density lipoprotein cholesterol (HDL-C), than their age- and race-matched able-bodied counterparts.5 These findings suggest that nontraditional risk factors may at least partially explain their increased disease rates. C-reactive protein (CRP), a nontraditional risk factor, is a marker of inflammation that has been shown to predict CVD across populations.6, 7, 8, 9, 10 The American Heart Association recommends the measurement of CRP for CVD risk in certain populations.11 Few studies have examined CRP concentrations in SCI populations, and these have not included appropriate comparison groups and/or did not control for other known influences on CRP (eg, waist, race, age, smoking).12, 13, 14 HDL-C has antioxidant15 and anti-inflammatory16 functions; however, in conditions of chronic inflammation, these functions become defective.17, 18 In patients with severe inflammation, such as rheumatoid arthritis, lower HDL-C has been associated with higher CRP and subclinical atherosclerosis.19 Among SCI populations, lower HDL-C has been well established for over 2 decades20, 21; however, the relationship between HDL-C and CRP in this population is unknown. People with tetraplegia tend to have lower HDL-C than those with paraplegia; however, the completeness of injury does not impact HDL-C levels.22 Whether the completeness or level of injury is associated with different CRP concentrations has not been examined. The purpose of this study was to examine whether people with SCI have elevated CRP compared with the able-bodied population and to assess the association of CRP with HDL-C and the influence of completeness and level of injury on these parameters. Our study will provide new insights into assessing CVD risk by using traditional and nontraditional markers as well as disability-related risk factors. Understanding these parameters in SCI populations will assist in the development of more effective prevention strategies tailored to specifically target those with great CVD risk. Methods  A cross-sectional study design was used to investigate differences in inflammation and HDL-C status between SCI and able-bodied men matched for race and age. This matching criterion was used to control for variables that are known to influence the primary outcomes of interest including HDL-C and CRP.23, 24 Participants Men with SCI Men with SCI were recruited by using flyers and word of mouth from clinic waiting areas at the Rehabilitation Institute of Chicago at Northwestern University. Eligibility criteria for participation included being between 20 and 59 years old, at least 1 year post-SCI, and free of acute inflammatory diseases or infections (eg, urinary tract infection [UTI], pressure ulcer) or current medication use for these infections.25 At the time of recruitment, questions including “Do you currently have pressure sores or skin ulcers?” and “Do you currently have a urinary tract infection?” were used for screening. Persons who answered “yes” to either question or took medications for treating infections were excluded. Those who were reported to have a history of diabetes, hypertension, or high cholesterol were not excluded. Able-bodied men A dataset of able-bodied men was created from the 1999–2002 National Health and Nutrition Examination Surveys (NHANES)26 by using 1:1 matching on age and race with SCI participants. Eligibility and Subject Matching Eligibility criteria for the able-bodied included men without paralysis or amputation and having complete data on age, weight, waist circumference, HDL-C, CRP, and information on disease history and smoking status. Information on acute inflammatory diseases or infections was not available in NHANES. Therefore, no exclusion regarding infections was made. Matching was based on age (within 5y), sex, and race. The record having the same race and sex and minimum age difference with the SCI participant was selected as a control. To guarantee no duplication of controls, an able-bodied record was deleted after being selected from the NHANES dataset and no longer available for further matching. The dataset with able-bodied controls was vertically merged with the SCI dataset before analysis. This research was approved by the institutional review boards of Northwestern University and the University of Illinois at Chicago. Study Variables Demographic characteristics consisted of age, race, smoking status (yes, no), diabetes, hypertension, and high cholesterol history. The SCI men were also assessed for age at injury, time since injury, injury level, and completeness of injury. This injury-related information was mostly self-reported; when participants could not remember, their medical records were obtained for such information. The neurologic injury level was defined as the first spinal vertebral level (ie, C2-8, T1-12, L1-5, S1-5) that shows abnormal neurologic loss. For example, if a participant’s injury level was T11-12, his injury level was defined as T11. Because the sympathetic nervous system modulates the immune responses by inhibiting the production of proinflammatory cytokines and stimulates the production of anti-inflammatory cytokines27, 28 and a high level of SCI (injury at or above spinal cord T6) reduces sympathetic input, the injury level was classified as an injury site at or above T6 (yes, no). Complete injury was defined as no motor or sensory function in the anal and perineal region representing the lowest sacral (S4-5) cord; incomplete injury was defined as otherwise.29 Anthropometric measures included weight and waist circumference. Men with SCI were weighed in their wheelchair by using a wheelchair scale, a calibrated for accuracy daily to within 0.1kg, and then transferred out of their wheelchairs while their wheelchairs were weighed. The able-bodied men were weighed on a beam scale by using standardized methodologies used during NHANES data collection. Both SCI and able-bodied men wore minimal clothing when weights were obtained. The waist circumference measurement technique differed between the groups. The supine waist was obtained for the SCI men because standing waist circumference is not feasible.30 The men in NHANES had their waist circumference assessed while standing. Recumbent and standing measures of waist circumference are highly comparable.31 Both groups had 3 measurements taken at the high point of the iliac crest to the nearest 0.1cm with minimal expiration, and the average was used for data analysis. All participants had blood samples obtained after a minimum of 9 hours of fasting. For SCI subjects, a reminder call at least 24 hours before their blood-draw appointment was made, and screening questions were repeated to make sure they were clear of infections for blood draw. If the participants answered “yes” to pressure ulcer or UTI when the reminder call was made, their blood-draw appointment was cancelled, and they were asked to reschedule with the researcher 1 week after finishing their antibiotic medication. The analysis of serum CRP and HDL-C in NHANES 1999–2002 has previously been described.32, 33 The measurement of CRP in SCI was conducted by Medical Research Laboratories International. High-sensitivity CRP concentrations in both NHANES and in blood samples from SCI men were measured by using latex-enhanced nephelometry.32 A cholesterol oxidase assay was used to measure serum HDL-C in SCI and able-bodied men. The physical activity level in SCI men was assessed by the Physical Activity Scale for Individuals with Physical Disabilities (PASIPD).34 This is a validated questionnaire with 13 items designed for people with physical disabilities, which asks the number of days and hours a day in the past 7 days subjects participated in recreational, household, and occupational activities. The total physical activity metabolic equivalents (METS) score for the PASIPD was created by multiplying the average hours per day for each activity by an METS value associated with the intensity of the activity and summing over activities 2 through 13.35 By using this scoring procedure, the mathematically maximum possible score is 199.5 METS per day. Data Analysis The means and interquartile ranges (IQRs) were used for all continuous variables for consistency because outcome variables CRP and HDL-C were nonnormally distributed. Frequencies were used as descriptors for dichotomous variables including complete injury (yes, no); injury level at or above T6 (yes, no); current smoking (yes, no); and disease history (yes, no) of diabetes, hypertension, and high cholesterol. For differences between SCI and the able-bodied, a dependent t test and Wilcoxon signed-rank test were conducted for paired continuous variables, and the McNemar test was used for dichotomous variables. To eliminate the effect of disease history on CRP and HDL-C, we performed the Wilcoxon rank-sum test because an unequal sample size occurred in SCI and able-bodied patients when we excluded those who had a history for diabetes, hypertension, or high cholesterol. Conditional logistic regression was used to examine the odds ratios (ORs) and 95% confidence intervals (CIs) for having high CRP and low HDL-C in SCI versus able-bodied men while controlling for smoking and waist circumference. High CRP was defined as a CRP level of 3mg/L or higher36 and low HDL-C as an HDL-C level of less than 1.04mmol/L.37 For comparisons of complete versus incomplete and high (T6 and above) versus low (below T6) injury within SCI men, the Wilcoxon rank-sum test was performed to test differences for continuous variables and the chi-square test was used for dichotomous variables. Post hoc power analysis, which used the sample size and effect size in the study, was conducted based on the comparisons of 2 sample means difference for log CRP between SCI and the able-bodied and between complete versus incomplete and high versus low injury within SCI. To examine the association between CRP and HDL-C in SCI and able-bodied subjects, the Spearman rank correlation was first performed while controlling for age. Next, CRP and HDL-C tertiles were generated separately, and then subject characteristics for these tertiles were calculated correspondingly. Finally, the Jonckheere-Terpstra test and Kendall τ-b test were used to test for trends across tertiles for categoric and continuous variables, respectively. All continuous variables were examined for normality distribution, and nonnormal variables were log transformed to reach normality before the linear trend analysis. The multinomial logistic regression was performed to examine the association of complete injury with high versus low and medium versus low CRP tertile with and without controlling for age (continuous), smoking status (yes, no), weight (greater than median, yes/no), or waist circumference (greater than median, yes/no), and/or physical activity (greater than median, yes/no). Race was not included in the model because CRP was not different by race in the SCI men. Data were managed and analyzed by using SAS.b Given that a special subset was selected from the NHANES data as the able-bodied controls, the sample weights for the complex survey design were not applied in the matching and analysis. Results A summary of demographics, anthropometrics, and CRP concentration of the study population (129 age- and race-matched pairs) is presented in table 1. Over half (57%) of the men with SCI had a complete injury, and 39% had an injury at T6 or above. Despite similar age, smoking frequency, weight, waist circumference, and similar or lower prevalence of disease history (SCI vs able-bodied: 5% vs 2% for diabetes, P=.09; 11% vs 20% for hypertension, P=.04; 8% vs 19% for high cholesterol, P=.02), men with SCI had significantly greater median CRP (2.8mg/L vs 1.4mg/L) but lower median HDL-C (1.06mmol/L vs 1.16mmol/L) than their able-bodied counterparts. When those with a disease history of diabetes, hypertension, and high cholesterol were excluded, men with SCI (n=102) remained to have statistically higher median CRP (2.5mg/L vs 1.4mg/L, P=.003) but lower median HDL-C (1.06mmol/L vs 1.19mmol/L, P=.01) than their controls (n=87). After controlling for smoking and waist circumference, men with SCI had about 2 times of odds for high CRP (OR=2.29; 95% CI, 1.33–3.95) and low HDL-C (OR=1.81; 95% CI, 1.01–3.27) compared with age- and race-matched able-bodied men. They remained to be more likely to have high CRP (OR=2.26; 95% CI, 1.31–3.92) when low HDL-C was also controlled. Conversely, the OR for low HDL-C was no longer significant when high CRP was also in the model (OR=1.76; 95% CI, 0.92–3.34). Men with complete versus incomplete injury did not differ in age at injury, years postinjury, level of injury, age, smoking, weight, waist circumference, or HDL-C. However, those with complete injury had significantly higher CRP (median, 3.7mg/L vs 1.2mg/L) and a tendency toward a lower METS score (median, 10.0 METS vs 15.9 METS, P=.07) than those with incomplete injury. Those with a high injury level were more likely to smoke (68% vs 43%, P=.006) and tended to report a higher METS score (median, 15.9 METS vs 11.6 METS, P=.06). No differences in HDL-C or CRP were found between persons with different injury levels. However, post hoc power analysis indicated a 19% power for CRP difference between high versus low injury, despite a power of greater than 99% and 90% for CRP difference between SCI and the able-bodied, and complete versus incomplete injury, respectively. CRP was negatively associated with HDL-C (overall: Spearman ρ=−.26, P<.001; SCI: ρ=−.22, P=.02; able-bodied: ρ=−.24, P=.006), and the median CRP concentrations in low, medium, and high CRP tertiles were significantly higher in SCI subjects than the able-bodied (0.5, 2.2, 9.7mg/L in SCI vs 0.4, 1.5, 4.5mg/L in the able-bodied) (table 2). There was a significant trend toward greater CRP in subjects with lower HDL-C and a higher waist circumference and weight in both SCI and the able-bodied men. Among SCI men, elevated CRP was associated with a higher percentage of complete injury and lower physical activity. The median HDL-C in low, medium, and high tertiles was significantly lower in SCI than the able-bodied men (0.83, 1.07, 1.40mg/L in SCI vs 0.91, 1.16, 1.47mg/L in the able-bodied) (table 3). There was a significant trend toward a lower HDL-C in subjects with higher CRP, as well as higher waist circumference and weight in both SCI and the able-bodied men. Among SCI men, lower HDL-C was associated with higher percentage of smoking. Although the percentage of complete injury was higher and the METS score was lower in the lower HDL-C tertile, no significance was found for the trend test. The ORs and 95% CIs for elevated CRP in men with SCI are presented in table 4. Complete injury, age, smoking, weight, and waist circumference were all significant predictors for elevated CRP. After controlling for age, smoking, waist circumference, or weight, complete injury was still a significant predictor for elevated CRP. The odds of being in the medium versus low CRP tertile were over 5 times in those with complete injury compared with those with incomplete injury (OR=5.24; 95% CI, 1.92–14.32 vs OR=5.61; 95% CI, 2.00–15.72), and the odds of being in the high versus low CRP tertile were over 3 times in those with complete injury compared with those with incomplete injury (OR=3.21; 95% CI, 1.21–8.49 vs OR=3.65; 95% CI, 1.26–10.52) after controlling for weight or waist circumference, age, and smoking status. The association of complete injury with elevated CRP still remained significant when physical activity was also controlled in addition to weight, age, and smoking (n=101, OR=5.26; 95% CI, 1.55–17.90 vs OR=3.74; 95% CI, 1.17–11.92) or waist, age, and smoking (n=101, OR=6.03; 95% CI, 1.68–21.67 vs OR=4.77; 95% CI, 1.30–17.58). Discussion In the present study, we report that men with SCI who were free of infections had significantly higher CRP concentrations than their age- and race-matched able-bodied counterparts. These findings suggest their higher inflammatory state may contribute to their increased CVD morbidity and mortality. Our CRP concentrations were significantly lower than that reported by Frost et al12 (median, 2.8mg/L vs mean, 38.2mg/L), which probably is a reflection of their inclusion of subjects with UTIs. However, our CRP levels were very similar to those reported by both Lee et al14 (2.8mg/L vs 2.4mg/L) and Manns et al13 (2.8mg/L vs 3.0mg/L). Lee did not include whether subjects had complete or incomplete injuries, and Manns included only complete paraplegic men. Men with SCI frequently encounter pressure ulcers and UTIs, which cause an inflammatory response. We required all participants to be free of these conditions; however, sometimes participants developed one of these conditions between when they were recruited and when they were scheduled to have their fasting blood sample drawn, necessitating rescheduling to ensure the participant was infection free. It has been speculated that their predisposition to these events renders them chronically inflamed. The association of completeness of injury with CRP has not been reported. We found that men with complete injury had higher CRP than those with incomplete injury, and this was independent of waist circumference, weight, age, smoking status, and physical activity. In addition to their predisposition to pressure ulcers and UTIs, 1 possible biologic mechanism for elevated CRP in those with complete injury could be that those with complete injuries reported lower physical activity level, which is associated with higher CRP concentrations.38 Complete injuries involve loss of voluntary motor function below the SCI site and may have resulted in lower physical activity levels. Low HDL-C was associated with high CRP in both SCI and able-bodied men with identical magnitude, similar to previous findings in able-bodied populations.39, 40 HDL-C becomes proatherogenic in states of chronic systemic inflammation.17, 18 Accelerated atherosclerosis41 and decreased HDL-C levels associated with elevated CRP occur in severe states of inflammation such as in rheumatoid arthritis and systemic lupis.19 The HDL-C was more proinflammatory than HDL-C taken from controls, as measured by the capacity of HDL-C to prevent LDL-C oxidation.42 These studies suggest that other chronically inflamed populations may have dysfunctional HDL-C predisposing them to accelerated atherosclerosis. This hypothesis is supported by recent research showing increased coronary artery calcification, an indicator of atherosclerotic burden43 in an SCI population.44 Unfortunately, neither HDL-C nor CRP concentrations were reported in this study. We found that the likelihood for low HDL-C in SCI versus able-bodied men disappeared when high CRP was controlled in the model, suggesting that high CRP explains the low HDL-C in this population and is possibly the major risk factor for CVD risk. However, further research is needed to assess HDL-C function under high-level chronic inflammation in the SCI population. Study Limitations There are several limitations that warrant review. First, the cross-sectional study design does not examine cause-effect relationship between (complete) SCI and elevated CRP. Second, we were unable to exclude those able-bodied men who may have infections because of a lack of available data. In addition, more able-bodied controls had a disease history than SCI men. The lower CRP concentration in the able-bodied men minimizes this concern because the inclusion of infected persons or more people with disease history would have biased the results toward the null. Third, potential unrecognized UTIs among SCI might have biased our results. Additionally, subjects’ completeness of injury was based on self-reported information or medical record rather than on objective measures. Finally, sample size was fairly small and lacked adequate power to detect small differences between high versus low injury. Conclusions Independent of age, race, smoking, waist circumference, and weight, CRP was significantly higher in SCI than the able-bodied men and higher in complete versus incomplete injury. No conclusion can be made with respect to the association of CRP and level of injury because of a lack of power. High CRP explains low HDL-C in SCI versus able-bodied men. These findings suggest that an elevated CRP, possibly the major risk factor, together with decreased HDL-C may contribute to a greater incidence of CVD in the SCI population and warrant further study. Suppliers References 1. 1Kocina P. Body composition of spinal cord injured adults. 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44. 44Orakzai SH, Orakzai RH, Ahmadi N, et al. Measurement of coronary artery calcification by electron beam computerized tomography in persons with chronic spinal cord injury: evidence for increased atherosclerotic burden. Spinal Cord. In press. a Department of Human Nutrition, University of Illinois, Chicago, IL b Division of Nutritional Sciences, University of Illinois, Urbana-Champaign, IL c Spinal Cord Injury Acute Care and Rehabilitation, Northwestern Memorial Hospital and Rehabilitation Institute of Chicago, Chicago, IL.  Reprint requests to Carol L. Braunschweig, PhD, RD, Dept of Human Nutrition, University of Illinois, 1919 W Taylor St, Rm 650 (M/C 517), Chicago, IL 60612
Supported by the Agency for Healthcare Research and Quality, National Institutes of Health (grant no. R03HS011277-01). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. PII: S0003-9993(07)01593-6 doi:10.1016/j.apmr.2007.08.121 © 2008 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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