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Lone cryptogenic fibrosing alveolitis (CFA) is a progressive interstitial lung disease, with a median survival of 3 to 6 yr from the onset of dyspnea. CFA can be subdivided into prognostically significant histopathologic patterns, including nonspecific interstitial pneumonia (NSIP). We reviewed 78 patients with a clinicopathologic diagnosis of CFA, biopsied between 1978 and 1989, to evaluate the prevalence and prognostic significance of these histopathologic patterns, in particular NSIP. Biopsy appearances were reclassified by two pulmonary histopathologists as usual interstitial pneumonia (UIP) (47%), NSIP (36%), or desquamative interstitial pneumonia (DIP)/respiratory bronchiolitis-associated interstitial lung disease (RBILD) (17%). The kappa coefficient of agreement between pathologists was 0.49. In 67 cases, follow-up was complete to death or 10 yr after biopsy, with 50 deaths during a median follow-up of 42 mo (UIP, 89%; NSIP, 61%, DIP/RBILD, 0%). Survival was highest in DIP/RBILD and higher in NSIP than UIP, p < 0.0005. When analysis was confined to patients with UIP or NSIP, the mortality of UIP remained higher, p < 0.01, but the 5-yr survival in patients with fibrotic NSIP was only 45%, indicating that this histologic appearance is often associated with a poor outcome. A response to treatment was more frequent in DIP/RBILD than in NSIP (p < 0.01) or UIP (p < 0.0005). This study confirms the prognostic value of subclassifying patients with CFA according to histopathologic pattern. However, in patients with clinically typical CFA, a histologic diagnosis of fibrotic NSIP needs to be interpreted with caution and does not necessarily denote a good outcome.
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INTRODUCTION |
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ABSTRACT
INTRODUCTION
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The term "lone cryptogenic fibrosing alveolitis" (CFA), synonymous with idiopathic pulmonary fibrosis (IPF) (1), relates to an idiopathic progressive interstitial lung disease, with a mean survival from the onset of dyspnea of 3 to 6 yr (4). The entity of CFA is a major subgroup of the interstitial pneumonias, originally subdivided by Liebow and Carrington into usual interstitial pneumonia (UIP), desquamative interstitial pneumonia (DIP), bronchiolitis obliterans with interstitial pneumonia (some of which are now termed as bronchiolitis obliterans-organizing pneumonia [BOOP]), giant cell interstitial pneumonia (now thought of as a hard-metal pneumoconiosis), and lymphoid interstitial pneumonia (viewed by some as a lymphoproliferative disorder) (11). More recently, nonspecific interstitial pneumonia (NSIP) (12), respiratory bronchiolitis- associated interstitial lung disease (RBILD) (13), and diffuse alveolar damage, clinically termed acute interstitial pneumonia (AIP) when idiopathic (14), have been recognized as additional patterns (15, 16).
How these histologic patterns relate to patients with a clinical diagnosis of CFA remains contentious. Although DIP and UIP were believed by some to represent different stages of CFA, there is now a general consensus that DIP represents a separate entity to UIP and that CFA should be related to the latter histopathologic pattern. However, the relationship of NSIP to CFA remains harder to integrate. Although previous series have demonstrated a better outcome with a histopathologic pattern of NSIP than with UIP (17), the studied populations were not selected on the basis of a typical clinical presentation of CFA and were not entirely representative of the full spectrum of CFA encountered in clinical practice.
A pilot study of 30 patients who met clinical criteria for a diagnosis of CFA showed significantly better prognosis and response to treatment when diagnosed with a NSIP pattern rather than UIP (20). However, these patients were not representative of the larger population of CFA patients described in keynote historical series (5). In the computed tomography (CT) era, thoracoscopic biopsy in suspected CFA has been increasingly reserved for the minority of patients with atypical CT features; thus, patients with typical disease are increasingly excluded from histologic studies. The aim of the present study was to evaluate the clinical significance of histopathologic reclassification in the whole spectrum of CFA encountered in clinical practice, before the advent of CT had resulted in a major selection bias.
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Between January 1, 1978 and November 31, 1989, 205 patients met all four clinical criteria for a diagnosis of lone CFA: (1) bilateral basal crackles or widespread crackles, most prominent at the bases; (2) abnormalities compatible with bilateral lung fibrosis on chest radiography, in a distribution typical of fibrosing alveolitis; (3) a restrictive functional defect (reduction in TLC below 80% of predicted normal associated with a restrictive FEV1/FVC ratio) or isolated reduction in diffusing capacity of the lungs for carbon monoxide (DLCO); and (4) absence of occupational or environmental cause for pulmonary fibrosis (6). Open lung biopsies were performed in 108 patients: 81 were reviewed (the remaining 27 cases were unavailable or the biopsy had been performed more than 6 mo before referral). Three cases were excluded on histopathologic reevaluation: one was reclassified as sarcoidosis, known to mimic CFA both clinically and radiologically (21), and two were reclassified as chronic obstructive pulmonary disease (COPD) with associated minor interstitial fibrosis. This left 78 cases with histopathologic appearances consistent with UIP, NSIP, DIP, or RBILD. There was no overlap between these 78 patients and patients included in previous histologic studies of CFA from our institution (7, 20); the study population makes up a subgroup of an earlier nonhistologic study in which survival in CFA was compared with survival in the fibrosing alveolitis of systemic sclerosis (22).
Slides were reviewed independently by two pulmonary histopathologists (A.G.N., T.V.C.), without knowledge of the clinical data. All sections had been routinely stained with hematoxylin-eosin, with additional staining using elastin van Gieson stains. In 22 of 81 cases, biopsies were taken from two separate areas, in 18 cases from separate lobes of which one was a lower lobe. Both biopsies were evaluated together and, when classification differed between the pathologists, a consensus opinion on the overall histopathologic pattern was reached. The pattern of UIP was distinguished by a temporally heterogeneous pattern of ongoing lung injury (i.e., a variation in the age of fibrosis with foci of fibroblastic proliferation, where there was an abundance of plump spindle cells and little intervening collagen, immediately adjacent to areas of established fibrosis, these characterized by poorly cellular hyalinized collagen). Secondary features such as honeycombing and a subpleural distribution favored diagnosis of UIP. All other histopathologic patterns of interstitial pneumonia showed temporally uniform fibrosis when present, with a diffuse filling of alveoli by macrophages in DIP and a more peribronchiolar distribution in RBILD. In NSIP, the fibrosis and inflammation was either patchy or diffuse, but the pattern of lung injury remained temporally uniform. Cases of NSIP were subdivided into NSIP grade 1 (cellular interstitial pneumonia with little or no fibrosis), NSIP grade 2 (significant fibrosis consisting of mature collagen, sometimes with accompanying fibroblasts, these elements being present in constant proportions throughout the affected interstitium), and NSIP grade 3 (dense interstitial collagen deposition with or without derangement of architecture) (12).
Clinical data, including history of previous exposures, smoking, chronic disease, drugs, and clinical examination, were collected, either from the patient's notes or from general practitioner's records. Patients were categorized as nonsmokers, current smokers, or ex-smokers (a minimum of one cigarette a day for a minimum of 1 yr, stopping at least 3 mo before presentation). All but one patient (who was too compromised to undergo full lung function testing) were included in survival analysis. Changes in pulmonary function tests at 4 to 6 mo were evaluated (as close to 6 mo as possible). Lung function measurements had been performed at presentation and during the follow-up period, including FVC and DLCO. Results were expressed as percentages of values predicted from the subject's age, sex, and height. Lung volumes were measured using an Ohio water-seal spirometer (Ohio Instruments, Atlanta, GA). Measures of gas transfer (DLCO) were made by the single-breath technique using a P.K. Morgan respirometer (P.K. Morgan, Chatham, Kent, UK). Serial trends in pulmonary function tests at follow-up were defined as improvement (a rise of over 15% in FVC or DLCO), decline (a fall of over 15% in FVC or (DLCO), or stability (a change of less than 15%) (23, 24).
For treatment effects, we analyzed all patients who were on no treatment (n = 56) or low-dose prednisolone (< 10 mg daily, n = 3) at the time of referral, who subsequently went on to receive high-dose prednisolone (60 mg daily for 4 wk, then reducing by 5 mg/d each week to a maintenance dose of 20 mg on alternate days) (n = 30, consisting of: UIP, n = 10; NSIP, n = 12; DIP, n = 8) or combination prednisolone/cyclophosphamide therapy (cyclophosphamide 100 to 120 mg/d; prednisolone 20 mg/d on alternate days) (n = 29, consisting of: UIP, n = 18; NSIP, n = 9; DIP, n = 2), as described previously (25). Nineteen patients were excluded (on high-dose therapy at referral, n = 7; died too soon to evaluate, n = 2 [one 10 d after biopsy, one with a cerebrovascular accident 2 mo after biopsy, before follow-up lung function tests were performed]; incomplete follow-up, n = 4; delay in starting treatment after biopsy or no treatment, n = 6).
Group comparisons were made using unpaired t tests (for normally distributed, continuous variables), Wilcoxon's rank-sum tests (for non-normally distributed variables), and chi-square statistics or Fisher exact tests as appropriate (for comparisons of proportions). Group survival was compared using proportional hazards regression with adjustment for the severity of disease, as judged by DLCO levels, and patient age at the date of biopsy (STATA data analysis software; Computing Resource Center, Santa Monica, CA) (26). A p value of less than 0.05 was regarded as statistically significant. Variation between pathologists in categorizing cases as NSIP, UIP, or DIP was quantified using the kappa coefficient of agreement (unweighted).
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Of the 78 patients who had a prior clinicopathologic diagnosis of CFA, 37 (47%) were reclassified as UIP, 28 (36%) as NSIP, and 13 (17%) as DIP/RBILD (Table 1). The kappa coefficient of agreement between the two pathologists overall was 0.49, and 0.26 in distinguishing between UIP and NSIP3 (the type of NSIP most frequently mistaken for UIP). Patients with DIP/ RBILD were younger than the other two groups (p < 0.00005 in both comparisons) and were more likely to be female (p < 0.01 versus UIP, p = 0.12 versus NSIP), but did not differ in the severity of functional impairment. There were no other significant differences in age, male:female ratio, or the functional severity of disease between UIP and NSIP, although patients with NSIP were slightly younger (p = 0.07) and had greater impairment of DLCO (p = 0.11). In two cases, the differential diagnosis included eosinophilic pneumonia, owing to an increase in the number of eosinophils within the chronic inflammatory cell infiltrate, but this diagnosis was not supported by accompanying clinical data, specifically the imaging and blood indices. Patients with NSIP had a slightly shorter duration of dyspnea at the date of biopsy than those with UIP, p = 0.07, but no trends were disclosed when patients with DIP/RBILD were compared with the other two subgroups.
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In 67 cases, follow-up was complete to death or 10 yr after biopsy. Follow-up was censored at less than 10 yr after biopsy in 11 patients, including five living overseas. There were 50 deaths during a median follow-up of 42 mo (UIP 33/37, 89%; NSIP 17/28, 61%; DIP/RBILD 0/13, 0%) (Table 1). As shown in Figure 1, survival was highest in DIP/RBILD/cellular NSIP and higher in fibrotic NSIP (NSIP2 and NSIP3) than in UIP, p < 0.0005; median survivals were 24 mo for UIP, 52 mo for NSIP and the median follow-up was 96 mo in the 13 patients with DIP/RBILD (all survivors). Differences in survival persisted, p < 0.0005, after controlling for age, smoking history, and percentage predicted DLCO immediately prior to biopsy. Mortality increased independently with increased age (coefficient 0.065/yr, 95% confidence interval [CI] 0.020 to 0.111, p = 0.005) and reduction in DLCO (coefficient 0.026/1% DLCO, 95% CI 0.004 to 0.049, p = 0.020), but was not independently linked to the smoking history. When analysis was confined to patients with UIP and fibrotic NSIP, the mortality of UIP remained significantly higher after adjustment for age, smoking history, and impairment of DLCO, p < 0.01; a higher mortality was independently associated with older age and greater impairment of DLCO (p = 0.06 and p = 0.03, respectively), but not with the smoking history.
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As shown in Figure 2, survival in patients with NSIP was highest in NSIP1 (n = 3) and higher in NSIP2 (n = 12) and in NSIP3 (n = 13) than in UIP (p = 0.02 and p < 0.05, respectively). After adjustment for age, smoking history, and percentage predicted DLCO, survival in NSIP2 (p < 0.01) and NSIP3 (p = 0.03) remained significantly higher than in UIP. Responsiveness to treatment was more frequent in DIP/ RBILD than in NSIP (p < 0.01) or UIP (p < 0.0005) (Table 1); however, there were no significant differences between UIP and NSIP, either in responsiveness to treatment (3/28 versus 6/21), or in the prevalence of decline in lung function (8/28 versus 2/21), at 4 to 6 mo.
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The aim of this study was to assess the value of the histologic reclassification of cases presenting with a clinical diagnosis of CFA. The results are notable for two features. First, the proportion of patients found to have NSIP was higher than in other series (Table 2) (17), but this finding was wholly ascribable to the presence of a large subgroup with fibrotic NSIP. More importantly, the present series documents a much worse outcome in NSIP at 5 yr than previously reported, although survival in NSIP was significantly better than in UIP.
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It is likely that the poor outcome in NSIP in the present study, compared with previous series, largely results from the selective inclusion of patients meeting clinical criteria for a diagnosis of CFA and undergoing open lung biopsy. In previous series of patients with subgroups of NSIP and UIP, clinical criteria for a diagnosis of CFA were not inclusion criteria (17) or a highly selected subgroup were studied (20). Nagai and coworkers reported a cohort in which many patients had clinical and, particularly, radiologic findings suggestive of cryptogenic organizing pneumonia (18). Similarly, in the series of Bjoraker and coworkers, 20% of patients did not have crackles and would not have been included in the large historical series, in which the survival characteristics of the clinical entity of CFA/ IPF were defined (17). Travis and coworkers viewed their cases of fibrotic NSIP as "a group of miscellaneous non-UIP fibrosing disorders of diverse aetiologies" (19); they did not suggest that the clinical entity of CFA was selectively evaluated in their study. More recently, CT scanning has introduced a major selection bias in the decision to proceed to biopsy: Daniil and coworkers emphasized that the selection of patients for biopsy was heavily influenced by "some unusual features in their clinical and particularly radiographic work-up" (20).
Thus, in previous histologic series of patients with UIP and NSIP (17) the spectrum of clinically typical CFA was not selectively studied. The major strength of the present study is the description of a cohort in which the diagnosis of CFA was made by clinicians who had defined the entity of CFA in earlier keynote historical series (6, 7), at an institution in which an open lung biopsy was performed whenever possible, by protocol. Thus, our findings can be applied to the classic clinical entity of CFA, widely encountered in routine respiratory practice. The relatively poor prognosis in fibrotic NSIP in the present study highlights the dangers of extrapolating previous reports of a good outcome associated with NSIP to patients with clinically typical CFA.
NSIP had most likely been described before Katzenstein and Fiorelli's study (12), with Kitaichi proposing an "unclassified" group of interstitial pneumonia in 1990 (27), and histopathologic patterns whose descriptions equate to NSIP being described in other series relating response to treatment in patients with CFA (28). Indeed, the term nonspecific interstitial pneumonitis had been used prior to 1990 in relation to patients with human immunodeficiency virus (HIV) infections (29) but, in relation to idiopathic or connective tissue disorder-related interstitial pneumonias, "NSIP" only became established as a diagnostic term after Katzenstein and Fiorelli's study. They described a group of cases of interstitial pneumonia, which could not be classified according to the recognized subsets at that time. They were, however, particular in stating that this was not a specific disease entity, because some cases were associated with collagen vascular diseases, some with exposure to environmental allergens, and some had a history of acute lung injury, the histopathologic pattern perhaps reflecting incomplete resolution of diffuse alveolar damage. Despite this, the pattern that they described showed greater response to treatment and a more favorable prognosis than patients with a histologic pattern of UIP (12).
With incorporation of the histopathologic pattern of NSIP into the classification of idiopathic interstitial pneumonias (16), we wished to assess Katzenstein and Fiorelli's grading system in a group of patients with idiopathic NSIP. When cases were subgrouped according to the degree of fibrosis, there were significant differences between the fibrotic (NSIP2 and NSIP3) and nonfibrotic (NSIP1) groups, although the number of cases classified as NSIP1 is small. These data especially support the recent findings of Travis and coworkers who found that cellular, i.e. nonfibrotic NSIP, had a significantly better prognosis than patients with fibrotic NSIP (19), and that fibrotic NSIP had a worse prognosis than DIP/RBILD. However, our 5-yr survival for fibrotic NSIP (grades 2 and 3 combined) was much worse than that described by Travis and coworkers (45% versus 90%), and this difference in outcome is likely to reflect the nature of the population in the present study, that of clinically typical CFA.
In this series, cases were also reviewed independently by two histopathologists, in order to evaluate the reproducibility of the classification system. A kappa value of 0.49 is regarded as clinically acceptable and is comparable to that seen in the scoring of CT patterns in CFA (i.e., which morphologic pattern predominates) (30), but it highlights the fact that, despite its "gold standard" status, assessment of open lung biopsies is subject to interobserver variation when CFA is subgrouped into patterns of interstitial pneumonia. Furthermore, the kappa value for distinguishing between UIP and NSIP3 was only 0.26, underlying the difficulty in making this distinction in some cases. With the histopathologic differences at the fibrotic end of the NSIP spectrum less well defined than at the cellular end, our analyses support suggestions that it may be more appropriate to refer to such cases as "end-stage lung" or "interstitial lung with honeycomb change" rather than attempting further subclassification (16).
A response to treatment was more frequent in DIP/RBILD than in NSIP and UIP, supporting the contention that the small percentage of patients with CFA who responded to corticosteroid therapy in previous studies may have had patterns other than UIP (7). It has been observed that an early response to treatment (7) and improvement or stability in lung function indices after 1 yr of treatment (31) are powerful predictors of long-term survival in CFA. Our data show that, whereas responsiveness to treatment appeared to identify patients with a high chance of having DIP/RBILD, the distinction between NSIP and UIP was not strongly linked to changes in lung function indices after 4 to 6 mo of therapy. Thus, the clinician cannot rely upon short-term changes in clinical status to draw conclusions on likely histopathologic group, or longer-term survival to discriminate consistently between UIP and NSIP, when the majority of patients with NSIP have fibrotic disease. However, it is not yet clear whether prolonged aggressive treatment is more beneficial in fibrotic NSIP than in UIP.
Even before recognition of NSIP, variability in the clinical outcomes of patients with lone CFA had long been recognized, a finding which has often been accounted for by the idea that variations in the histologic patterns related to early and late phases of the same disease: in particular DIP being an early phase of UIP (4, 6, 32). However, most groups now regard UIP and DIP as distinct conditions (17, 35), a view supported by recent studies on the progression of CT findings in these two patterns: cases of DIP, which have a patchy distribution on CT, do not invariably progress to the characteristic subpleural distribution of UIP (36, 37). Our data support the latter view, not only because of the differences in prognosis between the subsets, but also because there were no significant differences between DIP and UIP in the duration of dyspnea before biopsy or severity of lung function impairment, indicating that DIP is unlikely to be a precursor of UIP. DIP is more appropriately grouped with RBILD, in view of their histopathologic and prognostic similarities (13, 38).
In conclusion, this study confirmed the prognostic value of subclassifying cases of lone CFA as UIP, NSIP, DIP, and RBILD. However, the outcome in patients with fibrotic NSIP was substantially worse than previously reported. This finding may be partially ascribable to difficulties in making the distinction between UIP and NSIP in advanced disease but is also likely to reflect the selection of patients considered to have the clinical entity of CFA, rather than the larger group of patients who are found to have NSIP at biopsy. Our findings indicate that in patients with clinically typical CFA, a histologic diagnosis of fibrotic NSIP needs to be interpreted with caution and does not necessarily denote a good outcome. Our study also emphasizes the importance of viewing NSIP in the context of the clinical presentation.
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Footnotes |
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Correspondence and requests for reprints should be addressed to Dr. A. G. Nicholson, Department of Histopathology, Royal Brompton Hospital, Sydney St, London SW3 6NP, UK. E-mail: a.nicholson{at}rbh.nthames.nhs.uk
(Received in original form March 9, 2000 and in revised form August 11, 2000).
Acknowledgments:
The authors would like to thank our colleagues in the
Department of Thoracic Surgery, led by P. Goldstraw, for undertaking the
biopsies and providing the tissue which made this work possible.
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References |
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REFERENCES
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D. Bouros, A. U. Wells, A. G. Nicholson, T. V. Colby, V. Polychronopoulos, P. Pantelidis, P. L. Haslam, D. A. Vassilakis, C. M. Black, and R. M. du Bois Histopathologic Subsets of Fibrosing Alveolitis in Patients with Systemic Sclerosis and Their Relationship to Outcome Am. J. Respir. Crit. Care Med., June 15, 2002; 165(12): 1581 - 1586. [Abstract] [Full Text] [PDF]
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R.L. Riha, E.E. Duhig, B.E. Clarke, R.H. Steele, R.E. Slaughter, and P.V. Zimmerman Survival of patients with biopsy-proven usual interstitial pneumonia and nonspecific interstitial pneumonia Eur. Respir. J., June 1, 2002; 19(6): 1114 - 1118. [Abstract] [Full Text] [PDF]
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K.R. Flaherty, G.B. Toews, W.D. Travis, T.V. Colby, E.A. Kazerooni, B.H. Gross, A. Jain, R.L. Strawderman III, R. Paine, A. Flint, et al. Clinical significance of histological classification of idiopathic interstitial pneumonia Eur. Respir. J., February 1, 2002; 19(2): 275 - 283. [Abstract] [Full Text] [PDF]
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M. J. TOBIN Tuberculosis, Lung Infections, and Interstitial Lung Disease in AJRCCM 2000 Am. J. Respir. Crit. Care Med., November 15, 2001; 164(10): 1774 - 1788. [Full Text] [PDF]
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A. G. Nicholson, A. U. Wells, D. o. H. R. Medicine, R. B. Hospital, London, and UK Nonspecific Interstitial Pneumonia-Nobody Said It's Perfect Am. J. Respir. Crit. Care Med., November 1, 2001; 164(9): 1553 - 1554. [Full Text] [PDF]
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K. R. FLAHERTY, W. D. TRAVIS, T. V. COLBY, G. B. TOEWS, E. A. KAZEROONI, B. H. GROSS, A. JAIN, R. L. STRAWDERMAN III, A. FLINT, J. P. LYNCH III, et al. Histopathologic Variability in Usual and Nonspecific Interstitial Pneumonias Am. J. Respir. Crit. Care Med., November 1, 2001; 164(9): 1722 - 1727. [Abstract] [Full Text] [PDF]
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W. W. DOUGLAS, H. D. TAZELAAR, T. E. HARTMAN, R. P. HARTMAN, P. A. DECKER, D. R. SCHROEDER, and J. H. RYU Polymyositis-Dermatomyositis-associated Interstitial Lung Disease Am. J. Respir. Crit. Care Med., October 1, 2001; 164(7): 1182 - 1185. [Abstract] [Full Text] [PDF]
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S. L. S. MacDonald, M. B. Rubens, D. M. Hansell, S. J. Copley, S. R. Desai, R. M. du Bois, A. G. Nicholson, T. V. Colby, and A. U. Wells Nonspecific Interstitial Pneumonia and Usual Interstitial Pneumonia: Comparative Appearances at and Diagnostic Accuracy of Thin-Section CT Radiology, December 1, 2001; 221(3): 600 - 605. [Abstract] [Full Text] [PDF]
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D. A. Lynch Nonspecific Interstitial Pneumonia: Evolving Concepts Radiology, December 1, 2001; 221(3): 583 - 584. [Full Text] [PDF]
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