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C-Reactive Protein Is an Independent Predictor of Severity in Community-acquired Pneumonia
James D. Chalmers, MBChB, MRCP (UK), Aran Singanayagam, MBChB, Adam T. Hill, MD, FRCPE
Department of Respiratory Medicine, Royal Inﬁrmary of Edinburgh, Edinburgh, Scotland, UK.
ABSTRACT BACKGROUND: C-reactive protein (CRP) is an acute phase protein synthesized by the liver primarily in response to interleukin-6. Initial studies have suggested that inﬂammatory markers may have a role in predicting severity. We investigated whether admission and day 4 CRP could predict severity in community-acquired pneumonia. METHODS: A prospective study was carried out over a 2-year period in a large teaching hospital. CRP was measured on admission and on day 4. The outcomes of interest were: 30-day mortality; need for mechanical ventilation and/or inotropic support; development of complicated pneumonia (lung abscess, empyema, or complicated parapneumonic effusion); the value of predictive tests were assessed using multivariate logistic regression. RESULTS: There were 570 patients included in the study; 30-day mortality was 9.6%. Low CRP levels showed a high negative predictive value for excluding 30-day mortality (CRP 10 mg/L 100%, CRP 50 99.1%, CRP 100 98.9%, CRP 200 94.9%). Low admission CRP levels 100 mg/L were independently associated with reduced 30-day mortality (odds ratio [OR] 0.18; 0.04-0.85), P .03; need for mechanical ventilation and/or inotropic support (OR 0.21; 0.14-0.4), P .002; and complicated pneumonia (OR 0.05; 0.01-0.35), P .003. A CRP that fails to fall by 50% or more within 4 days of admission is independently associated with increased 30 day mortality (OR 24.5; 6.4-93.4), P .0001; need for mechanical ventilation and/or inotropic support (OR 7.1; 2.8-17.8), P .0001 and complicated pneumonia (OR 15.4; 6.32-37.6), P .0001. CONCLUSIONS: Admission CRP 100 mg/L has reduced risk for 30-day mortality, need for mechanical ventilation and/or inotropic support, and complicated pneumonia. Failure of CRP to fall by 50% or more at day 4 leads to an increased risk for 30-day mortality, need for mechanical ventilation and/or inotropic support, and complicated pneumonia. C-reactive protein is an independent marker of severity in community-acquired pneumonia. © 2008 Elsevier Inc. All rights reserved. • The American Journal of Medicine (2008) 121, 219-225 KEYWORDS: Community-acquired pneumonia; C-reactive protein; Severity assessment
The initial clinical decision to admit or discharge a patient with community-acquired pneumonia can be difﬁcult. Data from the United States show the estimated average cost of inpatient care for community-acquired pneumonia is $7500, compared with $150-$350 for outpatient care.1 Evidence suggests that in many cases physicians overestimate the severity of community-acquired pneumonia, leading to unnecessary admissions, whereas others suggest that initial
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assessment may underestimate the potential severity of community-acquired pneumonia.2 This has led to the development of a number of severity scores and prediction rules. In the UK, the CURB65 prediction score has been in use since 20043 and is aimed to identify high-risk patients at risk of death and prioritize these patients for aggressive investigation, treatment, and care in High Dependency or Intensive Care environments, where appropriate. The Pneumonia Severity Index is used in the US and classiﬁes patients into 5 risk classes based on a number of clinical, demographic, laboratory, and radiological ﬁndings that predict 30-day mortality.4
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bronchiectasis. and complicated pneumonia. haemoptysis.6 On the basis of this evidence. both sites. update of the British Thoracic SoCommunity-acquired pneumonia ciety (BTS) guidelines does not was deﬁned as a history consistent recommend admission CRP as a CLINICAL SIGNIFICANCE with pneumonia (with 1 or more marker of severity. and standard blood tests are obtained for each patient admitted between February 2005 and February 2007 with a (full blood count. or pyrexia) acquired pneumonia.220 The American Journal of Medicine. the of the following: new-onset shortguidelines recommend measure● This study demonstrates that CRP 100 ness of breath. Patients present eiday 4 CRP can predict 30-day mortality. urea and electrolytes. duced primarily in the liver and is stimulated by cytokine The main inclusion criteria were presentation to hospital release. predictor of mortality in acutely ill patients.11 This has not been spefor mechanical ventilation and/or inociﬁcally examined in communitySite of Care and Data tropic support. March 2008 ical approval was obtained from the Lothian research ethics C-reactive protein (CRP) is an acute phase protein procommittee. and complicated acquired pneumonia. primary diagnosis of community-acquired pneumonia. Collection studies have examined whether a The Royal Inﬁrmary of Edinburgh low CRP can exclude severe comis a large teaching hospital serving munity-acquired pneumonia. need for menew-onset confusion. cough. need Table 1. sputum proment of CRP as a useful marker of mg/L on admission is associated with duction. liver function tests.7 A CRP that chanical ventilation and/or inotropic fails to fall by 50% or more within and new inﬁltrates on the chest support. 4 days of admission is indicative radiograph. respiratory rate. palliative care) . At ment of complicated pneumonia. A proforma is completed on admission that includes patient obMETHODS servations (blood pressure. temperWe conducted a prospective study of all adult patients ature). need for mechanther as self-referral to Accident and Emergency or via Genical ventilation and/or inotropic support. patients are reviewed by the medical team and the decision to admit or discharge the patient is made. primarily interleukin-6. and CRP).5. Vol 121. acute pulmonary embolism) Patients for whom active treatment is not considered appropriate (eg. No previous pneumonia. the authors re● C-reactive protein 100 mg/L provides pyema. However. pulmonary ﬁbrosis. sis. pulse. No 3.9. the 2004 absence of any exclusion criteria. Lothian and the South East of The aim of this study was to establish if admission and Scotland. Ethcoagulation proﬁle. chronic asthma) Immunosuppression (iatrogenic or acquired) Solid organ transplant Hematological disorders including hematological malignancy Chronic liver disease or cirrhosis Other acute co-morbid illnesses leading to physiological or metabolic derangement such that pneumonia severity assessment would be inappropriate (eg. and the developeral Practitioner referral to the Medical Assessment unit. chest pain. treatment failure in communityreduced 30-day mortality.8 It is well recognized that viewed patient records at fola high negative predictive value compalow-up clinic review to ensure that elevated concentrations of proinrable with CURB65 and PSI severity the discharge diagnosis was conﬂammatory cytokines correlate rules. C-reactive protein was mea- Table 1 Study Exclusion Criteria Hospital-acquired pneumonia—development of symptoms 48 hours after admission to hospital or discharge from an acute care facility within 14 days of admission Active thoracic or extrathoracic malignancy Conditions likely to cause diagnostic confusion or where chest radiograph changes are equivocal (eg. allergic bronchopulmonary aspergillosis) Chronic lung disease (chronic obstructive pulmonary disease. of adverse outcomes such as emIn addition.10 and it has been shown that 50% or more at day 4 is associated with Exclusion criteria are shown in elevated CRP is an independent increased risk of 30-day mortality. Small studies suggest that with a diagnosis of community-acquired pneumonia within an elevated CRP is relatively nonspeciﬁc and is not directly the study period (February 2005 to February 2007) and the related to severity. sidered to be pneumonia and that with severity and outcome of sep● Failure of C-reactive protein to fall by no exclusion criteria were present. UK with 900 inpatient beds.
Age was entered into the model as a continuous variable. Reason for Exclusion Hospital acquired pneumonia Active malignancy Immunosuppression Solid organ transplant Chronic liver disease Persistent shadowing on chest radiograph at follow-up Active treatment not appropriate Diagnosis other than pneumonia made at follow-up Diagnosis of lung cancer at follow-up Chronic lung disease sured on admission in all patients and repeated routinely at day 4. 570 358 62 (44-76) 62 (44-78) 48. Table 3 Population Characteristics Study Population Patients with Repeat CRP Measurement Up to Day 4 Baseline Characteristics Number Age (years) Sex . and smoking status.Chalmers et al Table 2 CRP as Predictor of Severity in Community-acquired Pneumonia 221 Patients Excluded from Study n 31 54 29 2 6 49 18 20 33 124 Statistical Analysis All data were analyzed using SPSS version 13 for Windows (SPSS Inc. Secondary outcomes were need for mechanical ventilation and/or inotropic support and development of complicated pneumonia (lung abscess. co-morbidity (chronic cardiac failure. sex. Chicago. Ill). 20. empyema. We used multiple logistic regression to compare the outcomes of interest in patients with elevated CRP ( 100 mg/L) compared with patients with lower CRP levels ( 100 mg/L). Data were obtained from patients’ case notes and from the hospital laboratory database. Reasons for exclusion are shown in Table 2. All patients received standard antibiotic therapy in accordance with British Thoracic Society guidelines.8%) 145 (25%) 87 (24. negative predictive value. 570 patients met the criteria and were included in the study.6%. Descriptive statistics of demographic and clinical variables are presented as median (interquartile range) unless otherwise stated. C-reactive protein was repeated at other times as clinically indicated. whereas other variables were coded as binary data. Complicated pneumonia developed in 7. diabetes mellitus).6%) 18 (5%) 204 (36%) 121 (33. The normal range for this assay is 10 mg/L. positive predictive value..9%) CRP C-reactive protein. patients spend 12-24 hours in the Combined Assessment Unit.7%) 51 (8.8%) 25 (4. chronic renal failure. Of all patients. To the baseline model we included age.2%) 49 (13.3% of patients.9%) 35 (9. All observations were taken in the Emergency Department within 4 hours of arrival.4%) 38 (6.% male Duration of admission (days) Chronic cardiac disease Cerebrovascular disease Chronic renal failure Diabetes mellitus Current smokers Exsmokers Nonsmokers Outcomes The primary outcome of interest was 30-day mortality. Characteristics are shown for the whole population and for those patients who had repeat C-reactive protein measurements available during the ﬁrst 4 days of treatment. Ill). or complicated parapneumonic effusion). Abbott Park. Sensitivity. The CRP assay reports results in mg/L.3%) 221 (39%) 150 (41.7 RESULTS There were 936 patients considered for inclusion during the study period. . Deﬁnitions for co-morbid conditions were as used in previous studies. Baseline characteristics of the study population are shown in Table 3.7% were discharged within 24 hours of admission. which provides intensive monitoring as well as noninvasive ventilation (bilevel or continuous positive airways pressure ventilation) and/or inotropic support. Clinical observations were taken from the admission pro-forma. The 30-day mortality rate was 9. For all analyses. Other studies examining CRP have used assays that report in mg/dL. This CRP assay is a standard assay used in British hospitals. a C-reactive protein level of 100 mg/L is equivalent to 10 mg/dL. stroke. speciﬁcity. from where they may be discharged or move on to a specialist ward. The Mann-Whitney U test was used for the comparison of 2 groups of continuous data.8% 48% 5 (2-11) 6 (3-11) 75 (13.4%) 16 (4.05 was considered statistically signiﬁcant. and the area under the receiver operator characteristic (ROC) curve was use for comparison of predictive tests. pneumonia severity (using CURB65 score). A 2 2 table using the Fisher’s exact test was used to compare readmissions before day 4. For purposes of comparison. C-Reactive Protein Measurement C-reactive protein was measured by ﬂuorescence polarization immunoassay using an Abbott TDX analyzer and Abbott reagents (Abbott Laboratories. a 2-tailed P value of . 13.4 Data presented as median (interquartile range) or % number of patients. Patients were enrolled in the study from both Accident and Emergency and the Medical Assessment unit. Critically ill patients may be admitted at any time to the Intensive Care Unit for invasive ventilation and/or inotropic support or to the high dependency unit.5% required invasive ventilation and/or inotropic support. Subsequently.
Vol 121. The area under the ROC curve for CRP was lower for 30-day mortality and need for mechanical ventilation and/or inotropic support.5% 15.6% pneumonia severity index. DISCUSSION In this study.5. A C-reactive protein level that fails to fall by 50% or more within 4 days is associated with increased 30-day n 70 82 106 132 180 115 39 Mortality (30-Day) 18.9-2. increased rates of mechanical ventilation and/or need for inotropic support. P .7% 0.8% 18.05.6%) compared with 4 patients readmitted within 7 days in the CRP 100 mg/L group (8. 6.8% 10.5% 57% 9% PSI Class 1 2 3 4 5 Total n 81 131 108 159 91 570 30-Day Mortality (All Patients) 0% 1.0001) C-Reactive Protein Measurement on Discharge Before Day 4 There were 223 patients discharged before day 4.35.7% 7. 0.03) Need for invasive ventilation and/or inotropic support (OR 0. P . P . No 3.002) Complicated pneumonia (OR 0. a CRP 100 mg/L was independently associated with a reduced risk of: ● ● ● mortality. need for mechanical ventilation. Admission C-Reactive Protein as a Predictor of 30-day Mortality.5% 2. low CRP levels ( 100 mg/L) have high negative predictive values in excluding 30-day mortality. C-reactive protein 100 mg/L showed comparable negative predictive values for excluding 30-day mortality. a CRP that failed to fall by 50% or more at day 4 was associated with increased: ● ● ● 30-day mortality (OR 24. 0.8.32-37. 0.2% 9.21.2% 0. but was higher for predicting complicated pneumonia.8% 4-10% 27% 10. P . P . In addition. and a higher incidence of complicated pneumonia (Table 7).009).7% 35. There is no repeat C-reactive protein measurement available in 15 patients. and rates of complicated pneumonia increase with increasing levels of CRP on admission (Table 5).4% 3.9% 0% Complicated Pneumonia 21. Need for Invasive Ventilation and/or Inotropic Support. and/or inotropic support and complicated pneumonia.3% 3.14-0.8% 9. 6.2% 2.6-0. similar to previous studies by Lim et al3 and Fine at al4 (Table 4).18.8-17. need for invasive ventilation and/or inotropic support. and data were missing in 53 patients).1. repeat measurement of CRP at day 4 is shown to be a powerful marker Table 5 Admission C-Reactive Protein (CRP) and Adverse Outcomes C-Reactive Protein (mg/L) CRP 400 CRP 300-399 CRP 200-299 CRP 100-199 CRP 100 CRP 50 CRP 10 Invasive Ventilation and/or Inotropic Support 33.6% 0% 0% .0001) Need for invasive ventilation and/or inotropic support (OR 7.1-0.1% 0.6.4. P . 26 died or were admitted to the Intensive Care Unit within 4 days with no repeat measurement available.4% 0.003) Predictive Value of C-Reactive Protein for Outcome in Community-acquired Pneumonia C-reactive protein had high negative predictive values for excluding 30-day mortality up to levels 100 mg/L. On multivariate logistic regression. March 2008 Mortality and Existing Severity Scores (CURB65 and Pneumonia Severity Index) n 105 128 142 110 70 15 570 30-Day Mortality (All Patients) 0% 2.4. 78% of patients had a discharge CRP 100 mg/L.4.5% 15.222 Table 4 CURB65 Score 0 1 2 3 4 5 Total PSI The American Journal of Medicine. and complicated pneumonia.7%. The performance of CRP using a cut-off of 100 mg/L was compared with the existing severity criteria: CURB653 and the Pneumonia Severity Index scores4 (Table 6).85. 30-day mortality (odds ratio [OR] 0.6% National Studies (Lim et al)3 0. P .7% 1.6% 10. requirement for invasive ventilation and/or inotropic support.01-0. There was only 1 readmission within 7 days in this group (0.4-93.2% 3% 17% 41.04-0. On multivariate logistic regression.5% 15% 31% 47% 9. 2.9% 0% Admission CRP Combined with Day 4 CRP as a Predictor of Outcome Repeat CRP measurements at day 4 were available in 268 patients (223 were discharged in 4 days.3% 20% 13.6% National Studies (Fine et al)4 0. and Complicated Pneumonia Thirty-day mortality.0001) Complicated pneumonia (OR 15.7% 3.1% 0.
with some studies showing that TNF-alpha.7% 22. IL-6.2% 96.6% 99.87) 0.Chalmers et al Table 6 CRP as Predictor of Severity in Community-acquired Pneumonia 223 C-Reactive Protein as a Predictor of Severity Compared with CURB65 and Pneumonia Severity Index Scores PPV NPV 98.81) 0. however.6% 0.66-0.9% 41. Studies of cytokines and inﬂammatory markers in community-acquired pneumonia have not translated into clinically useful tests.9% 61.82) 0.80-0.6%* 0% 7.4% 94. no large studies have examined CRP and mortality in community-acquired pneumonia.71 (0.3% 26.1% 18.4% 97.9% 97. have shown that IL-6 levels correlate with BTS severity score15 and that IL-6 and IL-10 (an anti-inﬂammatory cytokine) correlate with Apache II score and are higher in patients ﬁtting the systemic inﬂammatory response syndrome criteria compared with patients who do not.7% AUC 0. AUC area under the receiver operator characteristic curve. Severity assessment is an important initial step in the management of community-acquired pneumonia.7%† 3.5% 71.74-0. *P . it would seem to follow that CRP also should be higher in patients with severe pneumonia.80) 0.55-0.75-0.4% 97.8% 33.3% 35.8% 97. n/a applicable.6% 14.5% 5. . and development of complicated pneumonia.87) Prediction of 30-day mortality CRP 100 mg/L CURB65 score 3 Pneumonia Severity Index 3 Prediction of mechanical ventilation and/or inotropic support CRP 100 mg/L CURB65 score 3 Pneumonia Severity Index 3 Prediction of complicated pneumonia CRP 100 mg/L CURB65 score 3 Pneumonia Severity Index 3 PPV positive predictive value.14 IL-6.3% 19.001.12 although tumor necrosis factor (TNF)-alpha.5% 18.5% 18.18 and that higher CRP levels result in longer duration of hospital stay and poorer clinical and radiological recovery.3% Speciﬁcity 34.74) 0.3% 20%* not C-Reactive Protein (mg/L) All patients All patients All patients CRP 100 CRP 100 CRP 100 CRP 100 50% 50% 50% Comparison between groups where CRP decreased by 50% or more compared with groups where CRP decreased by less than 50% or increased.3% 23. Despite this.9% 99% 99.6% 40.3%* Complicated Pneumonia 7. †P .8%* Invasive Ventilation/ Inotropic Support 13.8% 95.74) 0.10 Elevated CRP also has been shown to be associated with increased mortality in lower respiratory tract infection in primary care.0% 20.5% 37.80-0.13 Evidence of a relationship with severity has been conﬂicting.19 This is the ﬁrst study of this size to examine whether CRP levels predict 30-day mortality in community-acquired pneumonia.7% 7.3% 85. Studies have shown that elevated CRP in community-acquired pneumonia is independently associated with requirement for inpatient care.1% 94. IL-1.65) negative predictive value.6% 81.6% 97. and other cytokines are thought to be involved.7% 10.4%* 0% 15. C-reactive protein is an acute phase protein synthesized by the liver in response to tissue damage.83 (0.13 Others.3% 2.54 (0. in part because TNF-alpha and interleukin-6 are detectable in only a minority of patients.1% 40. Interleukin-6 (IL-6) is thought to be the primary trigger of CRP release.7% 22.5% 1.48-0.4%* 1. and soluble interleukin-2 receptor (IL-2R) do not correlate with severity.67-0. The Table 7 Admission C-Reactive Protein with Repeat Measurement at Day 4 n 570 175 93 83 13 92 80 Day 4 CRP n/a Decreased by 50% Increased/decreased by Decreased by 50% Increased/decreased by Decreased by 50% Increased/decreased by Mortality (30 Days) 9.8% 81.79 (0.5.71-0.3%* 0% 15.77 (0. CRP may therefore be a useful adjunct to clinical judgement in identifying low-risk patients. of treatment response—patients in whom the CRP level falls by 50% or more in 4 days have low rates of 30-day mortality.83 (0.01.17 As these cytokines are the primary stimulus for C-reactive protein release.9% 0.1% Sensitivity 96.7% 59. NPV 13. requirement for invasive ventilation and/or inotropic support.59) 0.70 (0.60 (0.76 (0.4%* 4. and IL-1 beta levels appear also to be higher in patients admitted to the Intensive Care Unit with pneumonia compared with those with less severe pneumonia.16 TNF alpha.
however. and complicated pneumonia should be of value to clinicians. elevated CRP 100 mg/L was associated not only with increased 30-day mortality.9 mmol/L .Nursing home residency Co-morbid illnesses Neoplastic disease Cerebrovascular disease Congestive cardiac failure Chronic renal disease Chronic liver disease Physical examination ﬁndings Altered mental status Respiratory rate 30/min Systolic blood pressure 90 mm Hg Temperature 35°C or 40°C Pulse 125/min Laboratory ﬁndings pH 7. requirement for invasive ventilation and/or inotropic support. The area under the ROC curve for CRP appears to be reduced primarily due to its lower speciﬁcity at high levels of CRP ( 200 mg/L). patients can be reclassiﬁed as low or high risk. This is supported in the literature.35 Blood urea 10. and the development of complicated pneumonia. This study found that around 30% of patients presenting with community-acquired pneumonia will fall into this category.7 mmol/L Sodium 130 mEq/L Glucose 13. The authors are not aware of any previous study that examined the predictive value of CURB65 or the Pneumonia Severity Index scores for complicated pneumonia. need for mechanical ventilation and/or inotropic support. C-reactive protein had.” and the ﬁnding in this study that patients in whom CRP falls by 50% or more in 4 days have low 30-day mortality. a CRP level that falls by 50% or more in 4 days indicates a low risk of 30-day mortality. the CURB65 score has become quickly established as an excellent tool for predicting patients at high risk of mortality. This study has shown that CRP 100 mg/L on admission has similar negative predictive values to the CURB65 and Pneumonia Severity Index scores for predicting 30-day mortality. or the development of complicated pneumonia.5 C-reactive protein has the potential to accurately identify a signiﬁcant proportion of patients presenting with community-acquired pneumonia as low risk. The PSI is a well validated prediction rule for 30-day mortality in CAP4 composed of the following characteristics: Demographics . objective severity assessment criteria are available only for The American Journal of Medicine. No 3. superior performance for predicting complicated pneumonia. In the UK. and studies suggest its performance is reduced when other outcome measures are considered.Age . but also was a marker of requirement for invasive ventilation and/or inotropic support and development of complicated pneumonia. C-reactive protein 100 mg/L provides a high negative predictive value comparable with CURB65 and PSI severity rules. where 25% of patients presenting with community-acquired pneumonia have a CRP 100 mg/L. APPENDIX 1 Severity Assessment The Pneumonia Severity index (PSI) and the CURB65 score were used to assess severity of illness of presentation. The high negative predictive value of CRP levels below 100 mg/L for each of these outcomes can reassure clinicians and has the potential to aid the initial decision to admit or discharge patients from hospital. Our study suggests that by using repeat measurements on day 4. C-reactive protein 100 mg/L has a high negative predictive value for 30-day mortality. and the ﬁnding that neither CURB65 nor the Pneumonia severity index can reliably predict complicated pneumonia requires further study. The ROC curves demonstrate that CURB65 and Pneumonia Severity Index had superior performance for predicting 30day mortality and need for mechanical ventilation and/or inotropic support.Sex . It is not intended or validated to predict other outcomes. CONCLUSION Low admission C-reactive protein levels 100 mg/L effectively excludes severe community-acquired pneumonia and can be used as an adjunct to clinical judgment to identify low-risk patients who may be safely discharged. Vol 121.20 In the present study. as recommended by the British Thoracic Society.224 difﬁculty of this initial assessment has led to development of a number of severity scores and indices to assist clinical decision-making. leading to a signiﬁcant improvement in risk stratiﬁcation. There is no reason why severity assessment should end at the hospital “front door. Currently. The authors feel that the negative predictive value of a test is the most clinically relevant. need for mechanical ventilation and/or inotropic support. One of the major advantages of CRP is that serial measurements can be taken as a marker of treatment response. suggesting that a low CRP can predict patients who may be safely discharged on clinical grounds. In patients admitted to the hospital. and for development of complicated pneumonia. March 2008 patients on admission. need for mechanical ventilation and/or inotropic support. The CURB65 score was designed and is validated to predict 30-day mortality.
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