The Red Cell Distribution Width as a Prognostic Indicator in Idiopathic Pulmonary Fibrosis
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1 CHEST The Red Cell Distribution Width as a Prognostic Indicator in Idiopathic Pulmonary Fibrosis Steven D. Nathan, MD, FCCP ; Taylor Reffett ; A. Whitney Brown, MD ; Chelsea P. Fischer ; Oksana A. Shlobin, MD, FCCP ; Shahzad Ahmad, MD ; Nargues Weir, MD, FCCP ; and Michael J. Sheridan, ScD Original Research DIFFUSE LUNG DISEASE Background: The course of idiopathic pulmonary fibrosis (IPF) is characterized by variable patterns of disease progression. The red cell distribution width (RDW) is a parameter that is routinely reported with all CBC counts. We sought to test the prognostic usefulness of this parameter in a well-defined cohort of patients with IPF. Methods: CBCs, demographics, and pulmonary function data from patients with IPF evaluated between January 1997 and June 2011 were collated. Patient outcomes were ascertained from the program s database and the Social Security Death Index. Results: There were 319 patients with IPF evaluated in whom baseline CBCs were available. The range in the RDW was 11.9 to 21.9 (median 14.1). There were 228 subjects with RDW values 15 (normal) and 91 patients with RDW values. 15. Patients with normal RDW values had a median survival of 43.1 months compared with 16.3 months for those whose RDW was. 15 ( P 5.001). There were 198 patients with available serial RDW data. Those patients who had a change in the RDW of less or greater than /mo had median survivals of 43.0 and 23.9 months, respectively ( P ). Conclusions: The RDW is a readily available laboratory test result that may provide important, independent prognostic information at baseline and follow-up in patients with IPF. Further studies are warranted to validate this as a biomarker for IPF outcomes, as well as to define the biologic basis for this association. CHEST 2013; 143(6): Abbreviations: Dlco 5 diffusing capacity of the lung for carbon monoxide; HgB 5 hemoglobin; IPF 5 idiopathic pulmonary fibrosis; MCV 5 mean corpuscular volume; PFT 5 pulmonary function test; RDW 5 red cell distribution width Idiopathic pulmonary fibrosis (IPF) is a potentially deadly disease with a median prognosis of approximately 3 years. 1,2 The disease course can be difficult to predict in individual patients with variable patterns of disease progression. Some patients remain stable Manuscript received June 1, 2012; revision accepted November 12, Affiliations: From the Advanced Lung Disease and Lung Transplant Program (Drs Nathan, Brown, Shlobin, Ahmad, and Weir; Mss Reffett and Fischer ), Department of Medicine; and the Inova Research Center (Dr Sheridan), Inova Fairfax Hospital, Falls Church, VA. Funding/Support: The authors have reported to CHEST that no funding was received for this study. Correspondence to: Steven D. Nathan, MD, FCCP, Advanced Lung Disease and Transplant Program, Inova Heart and Vascular Institute, 3300 Gallows Rd, Falls Church, VA 22042; steven. nathan@inova.org for long periods, others may demonstrate a stepwise pattern of progression, and there are those who may have acute unpredictable deteriorations. To discern patients with different prognoses, various pulmonary function test (PFT) parameters have been examined; however, baseline PFT parameters and their changes over time remain imperfect in risk stratifying individual patients. 1,3-6 Additional ancillary physiologic prognostic markers have been proposed, including measures of pulmonary hemodynamics and data derived from functional studies such as the 6-min walk test American College of Chest Physicians. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details. DOI: /chest Original Research
2 Prognostication of the disease is integral to disease management, including patient counseling and the timing of listing for transplantation. It is also important for the design, enrollment, and stratification strategies in clinical trials of therapy. Therefore, there remains a dire need for markers with improved performance characteristics. In this regard, readily available biomarkers, such as the brain natriuretic peptide and albumin, have been shown to impart prognostic information Additionally, there is a growing body of evidence attesting to the potential role of genomic profiling and description of peripheral blood proteins in delineating those patients with accelerated or slower disease courses, but these methods are costly and not commercially available. 14,15 The red cell distribution width (RDW) is a readily available parameter that is routinely reported with all CBC counts. It is a measure of the variability in circulating RBC size, calculated as the SD of the mean corpuscular volume (MCV) divided by the mean MCV and reported as a percent. Recent research has found the RDW to be a useful prognostic tool for various cardiovascular diseases, such as pulmonary arterial hypertension, congestive heart failure, and coronary heart disease Although small amounts of variation in RBC size are normal, significant variation has been linked to worse prognoses in these and other diseases. Indeed, the RDW has been found to be associated with increased mortality risk in the general population. 19 It has been previously proposed that an elevated RDW is caused by an underlying state of inflammation that induces changes in erythropoiesis, RBC circulation half-life, and RBC membrane deformability. 20,21 The relationship between the RDW and pulmonary disorders, including IPF, has not as yet been reported. Because of the pressing need for prognostic biomarkers in IPF, we sought to test the usefulness of the RDW in a well-defined cohort of patients with this disease. Materials and Methods The study cohort consisted of all patients with IPF evaluated in the Inova Advanced Lung Disease clinic between January 1997 and June The diagnosis of IPF was based on the 2000 American Thoracic Society/European Respiratory Society statement and the more recent 2011 American Thoracic Society/European Respiratory Society/Japanese Respiratory Society/Latin American Thoracic Association guidelines. 22,23 Data from patients CBCs closest to the time of each patient s initial evaluation provided the patient s baseline data. Data from subsequent CBCs were also collated. The parameters that were collected from the CBCs included the hemoglobin (HgB), hematocrit, MCV, and RDW. Demographics including sex, BMI, age, race, pulmonary function data, and pulmonary hemodynamics (if available) were recorded. Patients who underwent lung transplantation were excluded. Patient outcomes were ascertained from the program database and from the Social Security Death Index. This study was approved by the Inova Institutional Review Board (IRB#08.155). The normal range for the RDW for our laboratory is 11.5% to 15%. Patients were divided into two groups based on whether they had an RDW on their baseline CBC (CBCbaseline ) of 15% (normal) or. 15% (elevated). Survival was compared between these groups. A survival analysis was also performed based on patient s rate of change in the RDW between the initial CBC and the most recent CBC for those patients in whom at least two CBCs were available. Survival was calculated from the time of the initial blood draw for this latter analysis. Statistics All demographic and pulmonary function data are presented as medians with ranges if continuous or as frequencies if categorical. Significance tests for comparisons between groups were based on Kruskal-Wallis test for continuous patient characteristics and x 2 test for categorical patient characteristics. Survival was calculated from the date of the CBC from which the RDW was obtained for all analyses. For change in the RDW, survival was calculated from the first of the two CBCs. Only all-cause mortality was considered in this study. Kaplan-Meier survival curves were calculated for the two RDW groups. The log-rank test was used to determine whether these curves were significantly different. Cox proportional hazards regression was performed for both the univariate and multivariate analyses, with specific focus on the independent effect of RDW on survival by controlling for potential confounding factors, including patient age, sex, FVC % predicted, and HgB. The RDW was analyzed in the Cox proportional hazard using a binary value and as a continuous variable. All calculations were performed using SAS software (v9.2, SAS Institute Inc). Results There were 319 patients with IPF seen over the course of 14 years in whom baseline CBC counts (CBCbaseline) were available. Most patients CBCbaseline measurements were within 90 days of their initial consultation (224 of 319, 70.2%), with a median absolute time difference of 28 days. Specifically, 188 of 319 (58.9%) patients had their CBCbaseline prior to their initial consultation, 55 of 319 (17.2%) had their CBCbaseline after their initial consultation, and 76 of 319 (23.8%) had their initial CBCbaseline and consultation on the same day. The range in the RDW in this cohort from their CBCbaseline (RDWbaseline) was 11.9 to 21.9, with a median for the group of The median survival for all patients from their baseline CBC count was 35.6 months. There were 228 subjects with RDWbaseline values 15 and 91 patients with RDWbaseline values. 15. The demographics of the two groups are shown in Table 1. Only 4.4% of the patients were on an immunosuppressive agent (mostly azathioprine) at the time of their evaluation, with no difference between the two groups ( P 5.125). No patients were started on azathioprine or cyclophosphamide after their initial evaluation. There was also no difference in smok ing history between the two groups. The high RDW group was younger, and their journal.publications.chestnet.org CHEST / 143 / 6 / JUNE
3 Characteristic Table 1 Baseline Characteristics of Cohort Stratified by RDW Status RDW 15% (n 5 228) RDW. 15% (n 5 91) No. Median Interquartile Range No. Median Interquartile Range P Valuea Age Sex, % men b Smoking history, % yes b BMI FVC % predicted FEV 1 % predicted FEV 1 /FVC % predicted D lco % predicted HgB ,.0001 MCV mpap, mm Hg D lco 5 single breath diffusing capacity for carbon monoxide; HgB 5 hemoglobin; MCV 5 mean corpuscular volume; mpap 5 mean pulmonary artery pressure; N 5 number; RDW 5 red cell distribution width. a Significance tests for comparisons between groups were based on Kruskal-Wallis test for continuous patient characteristics and x 2 test for categorical patient characteristics. Interquartile range: difference between the first and third quartiles. b Frequency provided for categorical variables. HgB levels were lower. In terms of their PFTs, there was no difference in the mean FVC % predicted between groups, but the FEV 1 % and diffusing capacity of the lung for carbon monoxide (D lco) % predicted of the high RDW group were lower. There was a significant difference in survival between the normal and high RDW groups. Those below the upper limit of normal had a median survival from the time of the first blood draw of 43.1 months vs 16.3 months for those whose RDWbaseline value was. 15 (P 5.001) ( Fig 1). Cox proportional hazards regression suggested that the risk of mortality was elevated in the group with RDW values. 15, compared with the group with RDW values 15, when controlling for age, sex, Hgb, and FVC % predicted (hazard ratio [HR] ; 95% CI, ; P 5.07) ( Table 2 ). Since this was borderline significant, we ran the same model with a RDW cutpoint of 16, which resulted in an HR of 1.489, which attained statistical significance (95% CI, ; P 5.04). However, when we ran the model with RDW as a continuous Figure 1. Survival of patients with idiopathic pulmonary fibrosis (IPF) stratified by RDW at baseline (normal RDW 15%, elevated RDW. 15%). RDW 5 red cell distribution width. variable, the HR decreased from 1.36 ( P 5.07) to 1.04 ( P 5.33). Of all the covariates, only the FVC % predicted was protective for the group with RDW values. 15 (HR ; 95% CI, ; P,.0001), with neither age, sex, nor Hgb attaining statistical significance in the adjusted model ( P 5.66, 0.85, and 0.75, respectively). Right-sided heart catheterization data were available in 103 patients, but because this represented only about one-third of the patients, pulmonary pressures were not incorporated in the model. It is noteworthy, however, that the patients with elevated RDW values did have significantly higher mean pulmonary artery pressure measurements ( Table 1 ). We further stratified patients into four approximate quartiles based on ascending RDW values. The resulting groups were constituted of patients with RDWbaseline values, 13, 13 to 14.9, 15 to 16.9, and 17. The median survival times for each group were 55.1, 41.6, 19.2, and months, respectively ( P 5.002) ( Fig 2 ), further supporting the hypothesis that RDW value is inversely proportional to survival. There were 198 patients with available serial RDW data. The mean time interval between these tests was 19.0 months (range, months). The median serial change in the RDW value ( RDW) corrected for time was /mo (range, to ). Those patients who had a RDW of /mo had a median survival of 43.0 months from the time of the first blood draw compared with those whose RDW was /mo, in whom the median survival was only 23.9 months ( P ) (Fig 3 ). Within the subgroup of patients with serial RDW data, Kaplan- Meier analysis from the time of the subsequent RDW (RDWfollow-up) data still discerned different survival rates between the two groups. Those with an 1694 Original Research
4 Table 2 Univariate and Multivariate Model Showing Hazard Ratios for the Variables Used Univariate Multivariate Variable HR (95% CI) x 2 P Value HR (95% CI) x 2 P Value Age 0.98 ( ) ( ) Sex 0.88 ( ) ( ) HgB 0.96 ( ) ( ) RDW 1.53 ( ) ( ) FVC % predicted 0.97 ( ) 22.3, ( ) 19.7,.0001 Significance tests for comparisons between groups were based on Cox proportional hazards regression. HR 5 hazard ratio. See Table 1 legend for expansion of other abbreviations. RDWfollow-up value. 15 had a median survival of 7.1 months vs 32.4 months for those whose RDW follow-up values were normal ( P ) (Fig 4 ). Discussion IPF is a potentially fatal condition that has a variable clinical course, making prognostication difficult in individual patients. Patient counseling and stratification of disease severity is usually based on physiologic parameters, consisting mostly of baseline and serial change in FVC % predicted and, to a lesser extent, D lco % predicted. The absence of a readily measureable biomarker that enables the differentiation of patients who are at higher risk of mortality is an unfortunate reality in IPF. In this study, we have demonstrated the usefulness of a routine, commonly measured, but little regarded biomarker in the form of the RDW. We show that the RDW value provides valuable prognostic information for patients with IPF. Our finding that patients with IPF with an increased RDW value are at heightened risk for all-cause mortality was determined by comparing the outcomes of patients with values above and below the normal range. This association was still present even after accounting for potential confounding factors, including age, sex, and HgB, which were not independently associated with mortality risk. As expected, the FVC % pre- dicted was significantly correlated with mortality risk. However, after accounting for this well-recognized prognostic variable, the RDW value still imparted independent prognostic information, albeit at a higher cutpoint of 16. There were differences in baseline characteristics of the two groups of patients, including lower FEV 1 % predicted, lower D lco, lower HgB, and higher incidence of pulmonary hypertension in the high RDW group. These parameters suggest more advanced disease, but severity was adjusted for in part by incorporating FVC % predicted in the multivariate model. The lower HgB may have resulted in greater erythropoiesis and hence higher RDW values; however, HgB was also adjusted for in the multivariate Cox model. Further supportive evidence of the prognostic value of the RDW level was provided by our quartile analysis, in which patients were divided into smaller groups based on ascending categories of RDW values. Specifically, we demonstrated decreasing median survival with each categorical increment in RDW in a doseresponse fashion. On the other hand, RDW value did not stand out as an independent risk factor for mortality when analyzed as a continuous variable, which likely reflects a threshold phenomenon with the signal muted by the majority of patients (71.5%) being within the normal RDW value range. In patients in Figure 2. Survival of patients with IPF stratified by RDW baseline quartiles (normal RDW, 13%, high normal RDW 13%-14.9%, elevated RDW 15%-16.9%, high elevated RDW 17%). See Figure 1 legend for expansion of abbreviations. Figure 3. Survival of patients with IPF with serial RDW values stratified by the median RDW monthly rate of change (change in RDW /mo vs RDW change /mo). See Figure 1 legend for expansion of abbreviations. journal.publications.chestnet.org CHEST / 143 / 6 / JUNE
5 Figure 4. Survival of patients with IPF with serial RDW values at least 3 months apart stratified by most recent RDW (normal RDW 15%, elevated RDW. 15%). See Figure 1 legend for expansion of abbreviations. whom serial CBC data were available, we determined that the most recent RDW values, as well as the rate of change in the RDW value, also differentiated survival. Therefore, our data demonstrate that RDW values obtained at the time of the initial diagnosis or at points beyond the initial diagnosis provide valuable prognostic information and may enable the identification of patients at higher risk for earlier mortality. The RDW is a measurement of the variability in the size of circulating RBCs and is commonly reported as part of a CBC. Higher values indicate greater variability in cell size, whereas lower values indicate more homogeneity. Although small amounts of variation in cell size are normal, significant variation has been linked to worse prognoses in several diseases, particularly cardiovascular disorders However, the pathophysiologic basis for the association between the RDW and IPF mortality is currently unknown. Elevated RDW values may be caused by an underlying state of inflammation that induces changes in erythropoiesis, RBC circulation half-life, and RBC membrane deformability. The higher mean pulmonary artery pressure in the high RDW group raises the possibility that the RDW value is a surrogate for underlying pulmonary hypertension, which could explain the higher mortality in this group. Indeed, the RDW has been shown to be a powerful predictor of outcomes in patients with idiopathic pulmonary arterial hypertension. 24 It is also possible that the RDW value might be a marker for other comorbidities, such as coronary artery disease, which may impact survival. 25,26 RDW value has been linked to age, nutritional status, smoking, and lung function. 27,28 However, none of these are likely to explain our findings; specifically, age and lung function were included in our multivariate analysis, and there was no difference in smoking history between the groups. Also, IPF is generally a condition that is not accompanied by severe malnutrition, and indeed the BMI, albeit a poor correlate, was similar between groups. It is also possible that the vascular distortion that accompanies the fibrotic process may cause a low-grade hemolysis, which results in a compensatory increase in erythropoiesis. The lower HgB levels noted in the high RDW group could also be due to lowgrade hemolysis. These mechanistic hypotheses are highly speculative and require further investigation in follow-up studies. This study has a number of limitations. First, it reflected data from one center accrued over a period of more than a decade, and our findings should be confirmed in other datasets, ideally in the context of future prospective studies. However, the likelihood of any time-dependent or other bias is low, since we used a predetermined laboratory value, ascertained outcomes from the date of the laboratory draw, and had a well-defined end point of survival. The time interval from among some of our cases within the serial RDW analysis was very short. This might have introduced a mortality bias, as the sickest patients were most likely to have serial blood draws, often times while in hospital perhaps toward the end of their disease course as reflected in the significant early mortality ( Fig 4 ). However, even though our statistical analysis was limited by smaller numbers, we were still able to demonstrate the value of serial change in the RDW as a prognostic indicator. We only included age, sex, HgB, and FVC % predicted in our multivariate analysis. Since our sample size was relatively small, including more variables in the model would have diminished the power of our analysis and increased the risk of a type 1 error. We chose only to include the FVC % predicted in this model rather than the D lco % predicted or FEV 1 % predicted because of the colinearity between these variables and the recognition of the former as a more validated marker of disease severity in IPF. The lower D lco % predicted and FEV 1 % predicted in the high RDW group could reflect a higher proportion of patients with combined pulmonary fibrosis and emphysema in the high RDW group. We were unable to assess for this radiographically because of the inconsistent availability of high-resolution CT scans for the study population. However the mean FEV 1 /FVC ratios between the groups was not statistically different, and there were only 3.3% of patients in the high RDW group with FEV 1 /FVC ratios, 70% vs 5.3% in the normal RDW group (data not shown). In any event, the influence of coexistent emphysema is controversial, with reports of both improved and worsened survival. 29 Another potential issue is that the end point was all-cause mortality as opposed to IPF-related mortality. However, we view this as a strength of the RDW measurement, since this enhances its usefulness and appeal in a realworld setting where patients with IPF commonly have multiple comorbidities. In the context of this study, we were not able to account for other comorbidities that could have been contributory factors and an alternate 1696 Original Research
6 explanation for the lower HgB noted in the high RDW group. Future validation studies should account for the influence of identifiable comorbidities that could impact survival. In summary, we have shown that the RDW value, a readily available, convenient, and cost-neutral test, is a useful prognostic tool in patients with IPF. This biomarker may prove to be a useful adjunct in allowing greater precision in our prognostication of patients with this unpredictable disease. It might have utility not only in the clinical setting but also in the research arena as a hematologic determinant of a high-risk population that is more susceptible to disease progression or death. Further studies evaluating the usefulness of the RDW value in IPF are encouraged, as are studies delving into the biologic basis of this association. Acknowledgments Author contributions: Dr Nathan and Dr Sheridan are the guarantors of the paper and take responsibility for the integrity of the work as a whole. Dr Nathan: contributed to inception of the idea, the analysis and interpretation of the data, and the writing of the paper. Ms Reffett: contributed to the acquisition and interpretation of the data and revision of the manuscript. Dr Brown: contributed to the acquisition and interpretation of the data and revision of the manuscript. Ms Fischer : contributed to the acquisition of the data and revision of the manuscript. Dr Shlobin: contributed to the acquisition and interpretation of the data and revision of the manuscript. Dr Ahmad: contributed to the acquisition and interpretation of the data and revision of the manuscript. Dr Weir: contributed to the acquisition and interpretation of the data and revision of the manuscript. Dr Sheridan: contributed to the analysis and interpretation of the data and writing of the paper. Financial/nonfinancial disclosures: The authors have reported to CHEST the following conflicts of interest: Dr Nathan has served as a consultant for InterMune, Gilead, Actelion Pharmaceuticals US Inc, GeNO LLC, and United Therapeutics Corporation. Dr Nathan has received grant funding from InterMune, Gilead, Actelion Pharmaceuticals US Inc, Boehringer Ingelheim GmbH, and FibroGen, Inc. Dr Nathan has served on speakers bureaus for Gilead, Actelion Pharmaceuticals US Inc, and United Therapeutics Corporation. Dr Shlobin has served on speakers bureaus for Actelion Pharmaceuticals US Inc and United Therapeutics Corporation. Drs Brown, Ahmad, Weir, Mss Reffett and Fischer, and Dr Sheridan have reported that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article. Other contributions: This work was performed at Inova Fairfax Hospital. References 1. Nathan SD, Shlobin OA, Weir N, et al. Long-term course and prognosis of idiopathic pulmonary fibrosis in the new millennium. Chest ;140(1): Fernández Pérez ER, Daniels CE, Schroeder DR, et al. Incidence, prevalence, and clinical course of idiopathic pulmonary fibrosis: a population-based study. Chest ;137(1): King TE Jr, Tooze JA, Schwarz MI, Brown KR, Cherniack RM. Predicting survival in idiopathic pulmonary fibrosis: scoring system and survival model. Am J Respir Crit Care Med ; 164 (7 ): Collard HR, King TE Jr, Bartelson BB, Vourlekis JS, Schwarz MI, Brown KK. Changes in clinical and physiologic variables predict survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med ;168 (5 ): Flaherty KR, Mumford JA, Murray S, et al. Prognostic implications of physiologic and radiographic changes in idiopathic interstitial pneumonia. Am J Respir Crit Care Med ; 168 (5 ): Latsi PI, du Bois RM, Nicholson AG, et al. Fibrotic idiopathic interstitial pneumonia: the prognostic value of longitudinal functional trends. Am J Respir Crit Care Med ; 168 (5 ): Lettieri CJ, Nathan SD, Barnett SD, Ahmad S, Shorr AF. Prevalence and outcomes of pulmonary arterial hypertension in advanced idiopathic pulmonary fibrosis. Chest ; 129 (3 ): Nadrous HF, Pellikka PA, Krowka MJ, et al. Pulmonary hypertension in patients with idiopathic pulmonary fibrosis. Chest ;128 (4 ): Lama VN, Flaherty KR, Toews GB, et al. Prognostic value of desaturation during a 6-minute walk test in idiopathic interstitial pneumonia. Am J Respir Crit Care Med ;168 (9 ): Swigris JJ, Swick J, Wamboldt FS, et al. Heart rate recovery after 6-min walk test predicts survival in patients with idiopathic pulmonary fibrosis. Chest ;136 (3 ): Leuchte HH, Baumgartner RA, Nounou ME, et al. Brain natriuretic peptide is a prognostic parameter in chronic lung disease. Am J Respir Crit Care Med ;173 (7 ): Song JW, Song JK, Kim DS. Echocardiography and brain natriuretic peptide as prognostic indicators in idiopathic pulmonary fibrosis. Respir Med ;103 (2 ): Zisman DA, Kawut SM, Lederer DJ, et al. Serum albumin concentration and waiting list mortality in idiopathic interstitial pneumonia. Chest ;135 (4 ): Selman M, Carrillo G, Estrada A, et al. Accelerated variant of idiopathic pulmonary fibrosis: clinical behavior and gene expression pattern. PLoS ONE ;2 (5 ):e /journal. pone Richards TJ, Kaminski N, Baribaud F, et al. Peripheral blood proteins predict mortality in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med ;185 (1 ): Hampole CV, Mehrotra AK, Thenappan T, Gomberg- Maitland M, Shah SJ. Usefulness of red cell distribution width as a prognostic marker in pulmonary hypertension. Am J Cardiol ;104 (6 ): Allen LA, Felker GM, Mehra MR, et al. Validation and potential mechanisms of red cell distribution width as a prognostic marker in heart failure. J Card Fail ;16 (3 ): Tonelli M, Sacks F, Arnold M, Moye L, Davis B, Pfeffer M ; for the Cholesterol and Recurrent Events (CARE) Trial Investigators. Relation between red blood cell distribution width and cardiovascular event rate in people with coronary disease. Circulation ;117 (2 ): Perlstein TS, Weuve J, Pfeffer MA, Beckman JA. Red blood cell distribution width and mortality risk in a community-based prospective cohort. Arch Intern Med ;169 (6 ): Bazick HS, Chang D, Mahadevappa K, Gibbons FK, Christopher KB. Red cell distribution width and all-cause mortality in critically ill patients. Crit Care Med ;39 (8 ): Lippi G, Targher G, Montagnana M, Salvagno GL, Zoppini G, Guidi GC. Relation between red blood cell distribution width and inflammatory biomarkers in a large cohort of unselected outpatients. Arch Pathol Lab Med ;133 (4 ): journal.publications.chestnet.org CHEST / 143 / 6 / JUNE
7 22. King TE, Costabel U, Cordier JF, et al. American Thoracic Society. Idiopathic pulmonary fibrosis: diagnosis and treatment. International consensus statement. American Thoracic Society (ATS), and the European Respiratory Society (ERS). Am J Respir Crit Care Med ;161 (2 pt 1 ): Raghu G, Collard HR, Egan JJ, et al ; ATS/ERS/JRS/ALAT Committee on Idiopathic Pulmonary Fibrosis. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med ;183 (6 ): Rhodes CJ, Wharton J, Howard LS, Gibbs JS, Wilkins MR. Red cell distribution width outperforms other potential circulating biomarkers in predicting survival in idiopathic pulmonary arterial hypertension. Heart ;97 (13 ): Gul M, Uyarel H, Ergelen M, et al. The relationship between red blood cell distribution width and the clinical outcomes in non-st elevation myocardial infarction and unstable angina pectoris: a 3-year follow-up. Coron Artery Dis ; 23 ( 5 ): Nathan SD, Basavaraj A, Reichner C, et al. Prevalence and impact of coronary artery disease in idiopathic pulmonary fibrosis. Respir Med ;104 (7 ): Grant BJ, Kudalkar DP, Muti P, McCann SE, Trevisan M, Freudenheim JL, et al. Relation between lung function and RBC distribution width in a population-based study. Chest ;124(2): Patel KV, Semba RD, Ferrucci L, et al. Red cell distribution width and mortality in older adults: a meta-analysis. J Gerontol A Biol Sci Med Sci ;65 (3 ): Jankowich MD, Rounds SI. Combined pulmonary fibrosis and emphysema syndrome: a review. Chest ; 141 ( 1 ): Original Research
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