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(Chest. 2004;125:522-526.)
© 2004 American College of Chest Physicians

Prognostic Implications of Histologic Patterns in Multiple Surgical Lung Biopsies From Patients With Idiopathic Interstitial Pneumonias*

Hannah Monaghan, MRCPath; Athol U. Wells, MD; Thomas V. Colby, MD, FCCP; Roland M. du Bois, MD; David M. Hansell, MD and Andrew G. Nicholson, DM

* From the Department of Pathology (Dr. Monaghan), Edinburgh University Medical School, Edinburgh, Scotland; Interstitial Lung Disease Unit (Dr. Wells and Prof. du Bois) and Departments of Radiology (Prof. Hansell) and Histopathology (Prof. Nicholson), Royal Brompton Hospital, London, UK; and Department of Pathology (Dr. Colby), Mayo Clinic, Scottsdale, AZ.

Correspondence to: Andrew G. Nicholson, DM, Department of Histopathology, Royal Brompton Hospital, Sydney St, London SW3 6NP, UK; e-mail a.nicholson{at}rbh.nthames.nhs.uk


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To determine the prevalence and prognostic significance of histologic discordance in multiple lung biopsy specimens obtained from patients investigated for suspected cryptogenic fibrosing alveolitis (CFA)/idiopathic pulmonary fibrosis (IPF).

Methods and results: Between 1984 and 2001, 64 patients undergoing investigation for CFA/IPF were identified in whom multiple biopsies were performed that showed either a pattern of usual interstitial pneumonia (UIP) or nonspecific interstitial pneumonia (NSIP). These cases were classified into three groups: concordant UIP-UIP (n = 25, 39.1%), discordant UIP-NSIP (n = 8,12.5%), and concordant NSIP-NSIP (n = 31, 48.4%). The discordant UIP group had survival, clinical, and physiologic features similar to those of the concordant UIP group, and prognosis in both concordant and discordant UIP groups was significantly worse than that of the concordant NSIP group (p = 0.02 and p = 0.04, respectively). The age of the concordant UIP group was higher than that of the concordant NSIP group, with the mean age of the discordant group being intermediate. There were no significant differences among the three groups in smoking history, duration of dyspnea, presence or absence of crackles, FVC, diffusion capacity of the lung for carbon monoxide, or PaO2.

Conclusions: Patients with discordant UIP-NSIP results on multiple biopsies show clinical behavior similar to those with concordant UIP-UIP and should be regarded as having CFA/IPF in the correct clinical context, rather than "idiopathic NSIP" for the purposes of management. Multiple biopsies should be considered in all patients in order to improve the prognostic information provided by lung biopsy.

Key Words: concordance • nonspecific interstitial pneumonia • usual interstitial pneumonia


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
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Cryptogenic fibrosing alveolitis (CFA)/idiopathic pulmonary fibrosis (IPF) affects approximately 20 per 100,000 of the population and is characterized by progressive disease, which has a poor response to treatment and progresses to death in > 50% of patients in 2 to 3 years.1 2 3 4 5 6 7 8 In the United Kingdom, the majority of patients with the clinical features of CFA/IPF undergo no histologic procedure, as the diagnosis is usually made on clinical and imaging grounds.9 However, when surgical lung biopsy is undertaken, usual interstitial pneumonia (UIP) is the most common histologic pattern, although other patterns from the recently adopted consensus classification system8 are also seen with varying frequency, the most recently defined being nonspecific interstitial pneumonia (NSIP).1 2 3 4 5 6 7 Identification of these patterns is prognostically useful and may change the clinicopathologic diagnosis from CFA/IPF,8 although exact clinicopathologic correlation for the histologic pattern of NSIP is imprecise due to its comparatively recent definition and likely multifactorial causation.8 10 Furthermore, it is now increasingly frequent for physicians to request biopsies from multiples sites in an effort to ensure that different stages of disease are sampled.11 This has led to identification of a cohort of cases where variable or "discordant" patterns6 are seen in tissue samples from multiple sites, and in particular patients in whom patterns of UIP and NSIP are present in either the same or different lobes. The aim of this study was to determine the prevalence and prognostic significance of multiple lung biopsies showing either concordance or discordance.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Histology
Surgical lung biopsy specimens from patients who underwent multiple biopsies for the investigation of subsequently proven CFA/IPF between 1984 and 2001 were reviewed by two pathologists, independently and without access to clinical data. Some cases are parts of cohorts reviewed in previous studies2 4 12 on the prognostic significance of interstitial pneumonias. In patients presenting before 1987, clinical criteria comprised the following: (1) bilateral predominantly basal crackles; (2) evidence of predominantly basal bilateral lung fibrosis on chest radiography, with no consolidation; (3) a restrictive functional defect (total lung capacity < 80% of predicted, in association with a restrictive FEV1/FVC ratio) or isolated reduction in DLCO; and (4) no known primary cause for pulmonary fibrosis.13 After 1987, CT criteria were added (predominantly basal/subpleural distribution; a mixture of reticular and ground-glass abnormalities, with traction bronchiectasis when ground-glass attenuation was prominent; the absence of consolidation or nodules).14 None of the patients had previous or coexistent lung or systemic diseases. All sections were routinely stained with hematoxylin-eosin, with additional slides stained with elastin van Gieson available if required. Diagnostic criteria from the American Thoracic Society/European Respiratory Society consensus classification system were applied.8 For each lobe, the two pathologists re-evaluated cases in which independent diagnoses differed, and a consensus was reached for the histologic pattern.4 One patient underwent three biopsies, and the remainder underwent two biopsies.

Sixty-four cases were identified, which were then subclassified according to criteria proposed by Flaherty et al6 as "concordant UIP," where a pattern of UIP was present in all biopsies; "discordant UIP-NSIP," where a pattern of UIP was present in at least one biopsy, and a NSIP pattern in at least one biopsy (intrapatient histologic variability); and "concordant NSIP," where a pattern of NSIP was present in all biopsies. Six other patients underwent multiple biopsies in which NSIP or UIP was present in one biopsy, three showed UIP–end-stage lung, two showed NSIP–end-stage lung, and one showed a combination of UIP and respiratory bronchiolitis. These cases were not included in analysis due to the small size of the groups.

Clinical Data
Clinical data, including physical examination, duration of dyspnea prior to biopsy, age at biopsy, smoking history, imaging features, and follow-up information, were collected from either the patient’s notes or from general practitioners’ records. Patients were categorized as nonsmokers, current smokers, or ex-smokers (a minimum of one cigarette a day for a minimum of 1 year, stopping at least 6 months before presentation). Survival was assessed from the time of biopsy, and all patients were included in the survival analysis.

Pulmonary Function Tests
FVC and diffusion capacity of the lung for carbon monoxide (DLCO) immediately prior to biopsy were expressed as percentages of values predicted from the subject’s height, age, and gender. Lung volumes were measured using an Ohio water-seal spirometer (Ohio Instruments; Atlanta, GA). Measures of DLCO were made by the single-breath technique using a PK Morgan respirometer (PK Morgan; Chatham, Kent, UK). Serial trends in pulmonary function tests at follow-up were defined as improvement (a rise of > 15% in FVC or DLCO), decline (a fall of > 15% in FVC or DLCO), or stability (a change of < 15%).15 16 In addition, PaO2 was measured at the time of biopsy. In some patients, a complete set of parameters was not available; in these cases, the parameters that were available were used.

Statistical Analysis
Group comparisons were made using unpaired t tests (for normally distributed, continuous variables), Wilcoxon rank-sum tests (for nonnormally distributed variables), and {chi}2 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).17 A p value of < 0.05 was regarded as statistically significant. Survival analysis was performed on those patients who underwent biopsy and were subsequently managed at our institution.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Of 64 patients with patterns of UIP and NSIP, 25 patients showed concordant UIP (group 1), 8 showed discordant UIP (group 2), and 31 showed concordant NSIP (group 3). Three patients with concordant NSIP were of cellular subtype, and 28 patients were of fibrotic subtype. In the discordant UIP group, two of eight patients with NSIP were of cellular subtype and six of eight were of fibrotic subtype. Table 1 shows the lobar distribution of these biopsies and indicates the percentage of biopsies performed that included the lower lobe. The percentages of biopsy samples obtained from the same lobe were 12.5%, 25%, and 23% for groups 1, 2, and 3, respectively; 91.6%, 87.5%, and 83.3% of groups 1, 2, and 3 had at least one biopsy sample obtained from a lower lobe. The number of lower lobe biopsies in the discordant cases (group 2) showed no difference in the rate of UIP and NSIP patterns. Patients in the concordant NSIP group had a significantly better survival than either discordant or concordant UIP (p = 0.02 and p = 0.04, respectively). There was no significant difference between the concordant and discordant UIP groups (p = 0.48; Fig 1 ); 75% of the concordant NSIP group were alive 5 years after biopsy, whereas only 17% of patients in the concordant and 37% of patients in the discordant UIP group were alive. This difference remained statistically significant after controlling for age, gender, smoking, duration of dyspnea, presence of crackles, PaO2, FVC, and DLCO in separate models.


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  		Table 1.. Frequency and Distribution of Biopsy Sites in Relation to Concordant and Discordant Patterns

 


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  		Figure 1.. Kaplan-Meier survival curves for patients with concordant UIP-UIP (n = 25), discordant UIP-NSIP (n = 8), and concordant NSIP-NSIP (n = 31), grouped by histologic patterns. Patients with concordant NSIP-NSIP had a significantly better survival than both discordant UIP-NSIP and concordant UIP-UIP (p = 0.02 and p = 0.04, respectively), but there was no significant difference between the concordant UIP-UIP and discordant UIP-NSIP groups (p = 0.48).

 
The baseline demographic and physiologic data are shown in Table 2 . Age differed among the three groups, with the age of concordant NSIP patients less than that of the discordant group and less again from the concordant UIP group. More women were seen in the concordant NSIP group than in the concordant UIP group, but this difference was not statistically different (p = 0.06). No significant differences were seen in smoking history, duration of dyspnea, the presence or absence of crackles on auscultation, FVC, DLCO, or PaO2.


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  		Table 2.. Characteristics of Patients Who Underwent Multiple Biopsies*

 

   Discussion
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 Materials and Methods
 Results
 Discussion
References
 
Although biopsy rates vary between countries and institutions in the investigation of idiopathic interstitial pneumonias, assignment of histologic pattern of interstitial pneumonia still provides significant prognostic and diagnostic data in patients undergoing biopsy. Increasingly, multiple biopsies are being undertaken in an effort to reduce sampling error,11 but there is only one published study6 that considers the implications of such data, the methodology of which was adopted for our own investigation. These previously published data showed a greater frequency of discordant UIP-NSIP, with 26% of patients in the study of Flaherty et al,6 as opposed to 12% in our own cohort. There is no obvious reason for this discrepancy, but it may relate to several factors. Firstly, our cohort of patients had more severe disease at presentation (mean DLCO, 46.9% predicted, as opposed to 55.7% predicted) and may therefore be more advanced and similar to UIP. Secondly, it may, in part, reflect the smaller number of cases in our study. Thirdly, 19.4% of our patients with multiple biopsies had tissue obtained from different sites in the same lobe, compared with 10.1% in the study of Flaherty et al.6

However, despite the lower frequency in our series, survival data were strikingly similar, with discordant UIP-NSIP behaving in similar fashion to concordant UIP, while concordant NSIP had a significantly better prognosis in both series. Furthermore, Flaherty et al6 also demonstrated that NSIP was seen in a younger age group than patients with discordant UIP, and this group in turn was younger than those with concordant UIP. These data are strikingly mirrored in our own study. The reason for these age differences is not known, but it has been suggested that some patients with a histologic pattern of NSIP who present with the clinical features of CFA/IPF represent early disease, with these patients later acquiring UIP.6 An alternative is that such cases of NSIP reflects areas of relatively "inactive" disease in CFA/IPF,10 in that one of the cardinal features in distinguishing UIP from NSIP is the presence of fibroblastic foci, and the extent of fibroblastic foci reflects disease progression and therefore disease activity.18 As such, a disease with variable activity and inactivity within the parenchyma would therefore show concomitant variations in histologic pattern (between UIP and fibrotic NSIP), the identification of which would be at the whim of sampling.19 Indeed, it may well be that both explanations for this discordance are true, in that the activity of CFA/IPF may increase with disease progression and the characteristic features of UIP would therefore become more apparent. Interestingly, patients with discordant UIP showed a high early mortality in this series, and a reason for this is not apparent. We considered the possibility that some of these patients may have had an acute exacerbation of IPF as a terminal event,20 but this was excluded on clinical grounds.

The combined mortality data for concordant and discordant UIP mirror previous publications from other institutions.1 3 5 7 As reported previously in analyses of this cohort, treatment was standardized, consisting of either high-dose prednisolone initially with subsequent reduction to a low maintenance dose, or standard combination therapy (low-dose prednisolone in combination with an immunosuppressive agent)2 4 12 ; these treatment protocols have never been shown to differ in efficacy. The treated course was similar in discordant and concordant UIP.

Our study also emphasizes that the practice of performing multiple biopsies at different sites is preferable to single biopsies, as a pattern of UIP is not uniformly present throughout the involved lung parenchyma. A significant number of patients with CFA/IPF may otherwise be inappropriately investigated as a result of being classified as NSIP on the basis of a single biopsy. It also provides evidence that a histologic pattern of NSIP is consistent with the clinicopathologic entity of CFA/IPF, if all other clinical data are consistent with the diagnosis.

One initially surprising finding in our study is that patients with concordant NSIP had a 75% 5-year survival, which is higher than survival for NSIP previously documented at this institution (50% 5-year survival).4 However, the cohort in the current study reflects practice between 1984 and 2001, as only single biopsies were performed prior to 1984, while the prior study encompassed cases from 1978 to 1998 in which several cases of NSIP were from patients who only underwent single biopsies. As such, this earlier study may well reflect the bias of sampling error for UIP, as discussed previously. In addition, surgeons tend to be reluctant to perform biopsy from two sites in "high-risk" patients with advanced disease; therefore, more severe cases of fibrotic NSIP may have been excluded from the current study on this basis. It is also notable that nearly 50% of patients in this series had a diagnosis of concordant NSIP-NSIP, which is a high number of cases. We believe that this in part reflects the bias of referral to a tertiary center of patients with significant ground-glass attenuation on high-resolution CT, in whom NSIP was more likely to occur. The presence of prominent ground-glass attenuation on high-resolution CT, giving rise to greater diagnostic insecurity, may also have acted as a stimulus to undertake two biopsies, thus increasing the proportion of patients with NSIP in this cohort. Other possible explanations include pathologist interobserver variation and the simple fact that there must always be a highest figure in a range of reported prevalence figures.

In conclusion, this study shows a 12% incidence of discordant UIP-NSIP in biopsies performed at multiple sites as part of diagnostic workup of patients with suspected CFA/IPF. These patients show clinical behavior similar to those with concordant UIP on biopsy and should be regarded as having CFA/IPF rather than idiopathic NSIP for the purposes of management. Multiple biopsy sites should be considered in those patients requiring a surgical lung biopsy for investigation of idiopathic interstitial pneumonias, provided they have sufficient lung function to tolerate the procedure, in order to improve prognostic information.


   Footnotes
 
Abbreviations: CFA = cryptogenic fibrosing alveolitis; DLCO = diffusion capacity of the lung for carbon monoxide; IPF = idiopathic pulmonary fibrosis; NSIP = nonspecific interstitial pneumonia; UIP = usual interstitial pneumonia

Received for publication November 15, 2002. Accepted for publication September 3, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Bjoraker, JA, Ryu, JH, Edwin, MK, et al (1998) Prognostic significance of histopathological subsets in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 157,199-203
  2. Daniil, ZD, Gilchrist, FC, Nicholson, AG, et al A histologic pattern of nonspecific interstitial pneumonia is associated with a better prognosis than usual interstitial pneumonia in patients with cryptogenic fibrosing alveolitis. Am J Respir Crit Care Med 1999;160,899-905[Abstract/Free Full Text]
  3. Nagai, S, Kitaichi, M, Itoh, H, et al Idiopathic nonspecific interstitial pneumonia/fibrosis: comparison with idiopathic pulmonary fibrosis and BOOP. Eur Respir J 1998;12,1010-1019[Abstract]
  4. Nicholson, AG, Colby, TV, du Bois, RM, et al The prognostic significance of the histologic pattern of interstitial pneumonia in patients presenting with the clinical entity of cryptogenic fibrosing alveolitis. Am J Respir Crit Care Med 2000;162,2213-2217[Abstract/Free Full Text]
  5. Travis, WD, Matsui, K, Moss, J, et al Idiopathic nonspecific interstitial pneumonia: prognostic significance of cellular and fibrosing patterns; survival comparison with usual interstitial pneumonia and desquamative interstitial pneumonia. Am J Surg Pathol 2000;24,19-33[CrossRef][ISI][Medline]
  6. Flaherty, KR, Travis, WD, Colby, TV, et al Histopathologic variability in usual and nonspecific interstitial pneumonias. Am J Respir Crit Care Med 2001;164,1722-1727[Abstract/Free Full Text]
  7. Flaherty, KR, Toews, GB, Travis, WD, et al Clinical significance of histological classification of idiopathic interstitial pneumonia. Eur Respir J 2002;19,275-283[Abstract/Free Full Text]
  8. Travis, WD, King, TE, Bateman, ED, et al ATS/ERS consensus statement of idiopathic interstitial pneumonias. Am J Respir Crit Care Med 2002;265,277-304
  9. Johnston, IDA, Prescott, RJ, Chalmers, JC, et al British Thoracic Society study of cryptogenic fibrosing alveolitis: current presentation and initial management. Thorax 1997;52,38-44[Abstract/Free Full Text]
  10. Nicholson, AG, Wells, AU Nonspecific interstitial pneumonia: nobody said it’s perfect. Am J Respir Crit Care Med 2001;164,1553-1554[Free Full Text]
  11. Qureshi, RA, Ahmed, TA, Grayson, AD, et al Does lung biopsy help patients with interstitial lung disease? Eur J Cardiothorac Surg 2002;21,621-626[Abstract/Free Full Text]
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