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Vol. 62. Issue 1.
Pages 23-30 (January 2007)
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Vol. 62. Issue 1.
Pages 23-30 (January 2007)
CLINICAL SCIENCES
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SEMIQUANTITATIVE ASSESSMENT OF SURGICAL LUNG BIOPSY: PREDICTIVE VALUE AND IMPACT ON SURVIVAL OF PATIENTS WITH DIFFUSE PULMONARY INFILTRATE
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622
Mauro Canziana, Alexandre de Matos Soeirob, Marcel Frederico de Lima Tagac, Cecília Farhata, Carmen Silvia Valente Barbasa, Vera Luiza Capelozzib
a Divisions of Respiratory Diseases and Pathology, Heart Institute (InCor), São Paulo University Medical School - São Paulo/SP, Brazil.
b Department of Pathology, São Paulo University Medical School - São Paulo/SP, Brazil.
c Division of Biostatistics, Federal University of São Paulo (Unifesp) - São Paulo/SP, Brazil.
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PURPOSE:

Surgical lung biopsy has been studied in distinct populations, mostly going beyond clinical issues to impinge upon routine histopathological diagnostic information in diffuse infiltrates; however, detailed tissue analyses have rarely been performed. The present study was designed to investigate the prognostic contribution provided by detailed tissue analysis in diffuse infiltrates.

METHODS:

Medical records and surgical lung biopsies from the period of 1982 to 2003 of 63 patients older than 18 years with diffuse infiltrates were retrospectively examined. Lung parenchyma was histologically divided into 4 anatomical compartments: interstitium, airways, vessels, and alveolar spaces. Histological changes throughout these anatomical compartments were then evaluated according to their acute or chronic evolutional character. A semiquantitative scoring system was applied to histologic findings to evaluate the intensity and extent of the pathological process. We applied logistic regression to predict the risk of death associated with acute and chronic histological changes and to estimate the odds ratios for each of the independent variables in the model.

RESULTS:

Impact on survival was found for male gender (P = 0.03), presence of diffuse alveolar damage (P = 0.001), and chronic histological changes (P = 0.0004) on biopsy. Thus, being male was associated with a slightly lower risk (O.R. = 0.18; P=0.03) of dying than being female. Death risk was increased 17 times in the presence of acute histological changes such as diffuse alveolar damage and 2.5 times in the presence of chronic histological changes.

CONCLUSION:

Detailed analysis of histological specimens can provide more than a nosological diagnosis: this approach can provide valuable information concerning prognosis.

KEYWORDS:
Surgical lung biopsy
Diffuse pulmonary infiltrate
Histopathological score
Diffuse alveolar damage
Prognosis
RESUMO
PROPOSIÇÃO:

A biópsia pulmonar cirúrgica tem sido estudada em populações distintas, geralmente abordando aspectos histopatológicos puramente diagnósticos em infiltrados pulmonares difusos, além de dados clínicos. Contudo, análises teciduais detalhadas em tais casos têm sido pouco exploradas. O presente estudo foi delineado com o intuito de se investigar a contribuição prognóstica fornecida pela análise histológica detalhada em infiltrados difusos.

MÉTODOS:

Foram examinados retrospectivamente os prontuários e biópsias pulmonares cirúrgicas de 63 pacientes maiores de 18 anos, com infiltrados difusos, de 1982 a 2003. O parênquima pulmonar foi dividido em 4 compartimentos histológicos: interstício, vias aéreas, vasos e espaços alveolares. Alterações histológicas de cada compartimento histológico foram então avaliadas de acordo com seu caráter evolutivo agudo ou crônico. Um escore semiquantitativo foi aplicado a achados histopatológicos com o intuito de se avaliar a intensidade e a extensão do processo patológico. Aplicamos regressão logística para predizer o risco de morte para alterações histológicas agudas e crônicas e para estimar a razão de probabilidades para cada uma das variáveis independentes do modelo.

RESULTADOS:

O impacto sobre a sobrevida foi observado para o gênero masculino (p=0.03), para a presença de dano alveolar difuso (p=0.001) e para alterações histológicas crônicas (p=0.0004) em biópsias. Assim, homens apresentariam menor chance (O.R. = 0.18; P=0.03) de morrer do que mulheres. O risco de morte foi 17 vezes maior na presença de alterações histológicas agudas como dano alveolar difuso e 2,5 vezes na presença de alterações histológicas crônicas.

CONCLUSÃO:

A análise detalhada de espécimes histológicos pode proporcionar maiores e mais valiosas informações de valor prognóstico do que o simples diagnóstico nosológico.

UNITERMOS::
Biópsia pulmonar cirúrgica
Infiltrado pulmonar difuso
Escore histopatológico
Dano alveolar difuso
Prognóstico
Full Text
INTRODUCTION

Diffuse pulmonary disease of uncertain etiology represents a diagnostic and therapeutic challenge in the general population. Most of the causes of pulmonary infiltrates can be diagnosed by noninvasive or minimally invasive means, such as transbronchial or transthoracic needle biopsies. However, when these efforts fail to provide a diagnosis or when a patient does not respond to appropriate therapy, a surgical lung biopsy may be required to assist in treatment efforts. This biopsy produces a histologic diagnosis in almost every case, but considerable controversy exists regarding whether the information provided justifies its routine use. Thus, similarly to the approach used from previously reported tumor recurrence studies1–5 and aiming for the effectiveness of treatment, there is great interest in identifying, as soon as possible, morphological parameters of surgical lung biopsies associated with the shortening of the patient’s life.

Because semiquantitative approaches have been thought to be important in evaluating the intensity and extent of pathologic processes,6–9 a scoring system has been considered to be potentially useful with surgical lung biopsies specimen markers.10,11 Several parenchymal alterations related to necrosis, degeneration, hyperplasia, neoplasia, inflammation/remodeling (fibrin and hyaline membranes deposition, polymorphonuclear and mononuclear cell infiltration, granulation tissue, granuloma, fibrocellular proliferation), and circulatory changes (edema, hemorrhage, congestion, thrombosis) have shown promise as useful markers.

Scoring systems have also been found to be significantly associated with survival,8,12 but there has been uncertainty about how best to design a scoring system. Hence, this project was undertaken to validate the importance of a scoring system and to explore the semiquantitative relationship between score and outcome; we also explored the relationship between the result of a scoring system and other epidemiological factors.

METHODSPatient selection

We examined the medical records of all patients who underwent surgical lung biopsy at our institution from 1982 to 2003 for age, sex, total hospitalization time, days from admission to the biopsy procedure, outcome, main clinical diagnosis, underlying disease, respiratory failure proven through clinical and or gasometric data (respiratory rate over 28 breaths per minute and/or PaO2 < 60 mm Hg and/or SpO2 < 90%, while breathing room air). From this group were selected those patients older than 18 years showing diffuse infiltrates on chest roentgenogram and whose hospitalization was not exclusively motivated by the biopsy procedure.

Over the period examined, 1657 surgical lung biopsies were performed at our institution; 63 patients (3.8%) met our study criteria. Thirty-two patients (51%) were men and 31 (49%) were women, with a mean age of 49 years (range, 18 to 92 years). Arterial blood samples for gas analysis taken during inspiration of room air in the 24 hours preceding SLB were obtained for 51 patients (81%), and 41 of them showed signs of acute respiratory failure. Table 1 lists the preexisting medical conditions in the study population. Thirty-three patients (52%) were immunocompromised, and 48 (76%) had at least 1 underlying disease. The mean time from admission to SLB was

Table 1.

Epidemiological data of the 63 patients studied

Case  Sex  Age  Total Hospitalization Time (days)  Underlying disease  Presence of immunosuppression factor  Outcome 
1  56  20  No  No  Dead 
2  48  32  No  No  Dead 
3  76  60  Renal and heart failure  No  Survived 
4  19  47  BMT (aplastic anemia)  Yes  Dead 
5  67  44  No  No  Survived 
6  55  17  Rheumatologic disease NOS  No  Dead 
7  52  27  Heart failure  No  Survived 
8  48  55  Crohn’s disease+ renal failure  No  Dead 
9  66  42  Rheumatoid arthritis  No  Dead 
10  37  44  SLE  No  Dead 
11  34  16  AIDS  Yes  Dead 
12  45  18  CML  Yes  Dead 
13  52  20  No  No  Survived 
14  21  38  Non-Hodgkin’s lymphoma  Yes  Survived 
15  30  37  No  No  Survived 
16  63  Carcinomatosis  Yes  Dead 
17  37  48  No  No  Dead 
18  51  22  Gastroesophageal reflux  No  Survived 
19  52  38  Liver cirrhosis  No  Survived 
20  46  26  Adenocarcinoma NOS  No  Dead 
21  34  CML  Yes  Dead 
22  49  19  Carcinomatosis  Yes  Survived 
23  23  21  Burns  No  Dead 
24  58  13  Adenocarcinoma NOS  Yes  Dead 
25  77  45  COPD  Yes  Dead 
26  36  20  BMT  Yes  Dead 
27  78  17  No  Yes  Survived 
28  54  SLE  No  Dead 
29  51  184  Wegener’s granumatosis  No  Dead 
30  57  33  Ischemic myocardiopathy  No  Dead 
31  21  42  SLE  No  Survived 
32  74  16  Congestive myocardiopathy  No  Dead 
33  55  91  Congestive myocardiopathy  No  Dead 
34  65  69  Sarcoidosis  No  Dead 
35  46  15  Wegener’s granumatosis  No  Survived 
36  52  76  No  Yes  Survived 
37  92  24  Ischemic myocardiopathy  No  Survived 
38  26  27  BMT (CML)  Yes  Dead 
39  53  98  Rheumatoid arthritis  No  Dead 
40  70  47  Non-Hodgkin’s lymphoma  Yes  Dead 
41  30  65  Colitis NOS  No  Survived 
42  82  22  Neoplasia NOS  Yes  Survived 
43  50  91  SLE  Yes  Survived 
44  57  38  Gastroesophageal reflux+DM 2  No  Survived 
45  65  37  Ischemic myocardiopathy+DM 2  No  Dead 
46  47  37  ALL  Yes  Dead 
47  32  16  ALL  Yes  Dead 
48  68  37  Hypertension  No  Survived 
49  53  26  Heart transplantation  Yes  Dead 
50  22  89  ALL  Yes  Survived 
51  18  BMT (ALL)  Yes  Survived 
52  76  36  Ischemic myocardiopathy  No  Dead 
53  55  17  Carcinomatosis  Yes  Dead 
54  25  47  No  No  Survived 
55  38  42  No  No  Dead 
56  37  84  CML  Yes  Dead 
57  36  10  Ischemic myocardiopathy  No  Survived 
58  36  14  Carcinomatosis  Yes  Survived 
59  73  34  No  No  Survived 
60  52  36  No  No  Survived 
61  31  49  SLE  No  Dead 
62  28  48  Aplastic anemia  Yes  Dead 
63  73  37  No  No  Survived 

AIDS: acquired immunodeficiency syndrome; ALL: acute lymphocytic leukemia; BMT: bone marrow transplantation; CML: chronic myelocytic leukemia; CPOD: chronic obstructive lung disease; DM: diabetes mellitus; NOS: no other specification; SLE: systemic lupus erythematous.

18 days (range, 0 to 61). The mean interval from SLB to hospital discharge or death was 18 days (range, 1 to 143), and the mean total hospitalization time was 39 days (range, 4 to 184). The overall death rate was 49%, and death rate for immunocompromised patients and for patients presenting respiratory failure or underlying diseases was 61%. Death occurred in 69% of patients presenting diffuse alveolar damage. Other details about the patients are summarized in Table 1.

Pathology review of surgical lung biopsy specimens

Samples were uniform and obtained generally in 2 different compromised regions; the entire sample was submitted to histological examination, generally on 2 different slides. The specimens were fixed in 10% phosphate-buffered formaldehyde solution and embedded in paraffin. Serial sections were cut (5 mm), deparaffinized, and processed according to routine tissue processing. Staining with hematoxylin and eosin was done for histological examination in all cases. In cases exhibiting proteinaceous intra-alveolar exudates, granulomas, or microabscesses, the following stains were used: silver stains and PAS for Pneumocystis and fungi, Ziehl-Neelsen for mycobacterium, and Gram stains for bacteria, respectively.

The biopsies were considered representative when the histological sections comprised at least 1 bronchovascular axis in continuity with septal interstitium, alveolar spaces, and peripheral interstitium. The lung parenchyma was then histologically divided into 4 anatomical compartments of reference: a) interstitium (septal, peripheral, and axial); b) airways (terminal and respiratory bronchioles); c) vessels (arteries, veins, and lymphatics); and d) alveolar spaces (including alveolar ducts) (Figure 1).

Figure 1.

(HE, 25X): Normal lung histology showing the 4 compartments studied: interstitium, alveolar spaces, airways and vessels. “PI”: peripheral interstitium; “SI”: septal interstitium; “AI”: axial interstitium; “*”: alveolar spaces; “TB”: terminal bronchioles; “A”: pre-acinar arterioles

(0.13MB).

Histological changes throughout the 4 anatomical compartments were then evaluated for temporal evolution into 2 groups as follows: 1) acute (necrosis, degeneration, edema, hemorrhage, congestion, thrombosis, fibrin deposition, hyaline membranes, and polymorphonuclear cells), and 2) chronic (hyperplasia, neoplasia, mononuclear cells, granulation tissue, granuloma, and fibrocellular proliferation) (Figures 2A to 2I and 3A to 3F).

Figure 2.

A (HE, 100X): parenchymal necrosis; B (HE, 200X): alveolar edema; C (HE, 100X): peripheral interstitium edema; D (HE, 200X): alveolar hemorrhage; E (HE, 200X): microvascular congestion; F (HE, 200X): acute vascular thrombosis; G (HE, 200X): alveolar fibrin deposition; H (HE, 200X): hialine membranes; I (HE, 200X): neutrophilic filling of alveolar spaces

(0.21MB).
Figure 3.

A (HE, 200X): pneumocytes hyperplasia; B (HE, 200X): neoplastic parenchymal infiltration; C (HE, 200X): mononuclear cell interstitial infiltrate; D (HE, 200X): granulation tissue filling alveolar spaces; E (HE, 200X): granuloma; F (HE, 200X): fibrosis (fibrocellular proliferation)

(0.15MB).
Semiquantitative assessment of histological compartments and histological changes

The severity of the acute and chronic histological changes in terms of the extent, intensity, and distribution were heterogeneous along the anatomic compartments. Therefore, the severity of these various acute and chronic histological changes was rated semiquantitatively according to the amount and severity of disease by the following histological score:

  • 0:

    absence of histological changes;

  • 1:

    parenchymal alterations in 1 to 25% of the tissue examined;

  • 2:

    parenchymal alterations in 26 to 50% of the tissue examined;

  • 3:

    parenchymal alterations in 51 to 75% of the tissue examined;

  • 4:

    parenchymal alterations in 76% to 100% of the tissue examined.

The sum of the scores for acute and chronic changes, respectively, represented continuous variables that we designated as acute and chronic indices.

Statistical Analysis

Logistic regression analysis was used to attain the best separation of survivors and nonsurvivors, discriminating between the two categories of patients according to clinical and histological variables. Evaluation of the predictive ability was determined by the percentage of patients correctly placed into the proper categories by the classification rules developed. In logistic regression, the probability of an event occurring is directly estimated. For more than 1 dependent variable, the model can be written:

Prob (event) = ez / 1 + ez

where Z is the linear combination of β0 (constant) and β1 to β7, the estimated coefficients of the independent variables (X1 to X7), and e is the base of the natural logarithms, (2.718, approximately), as shown below:

Z = β0 + β1X1 + β2X2 … β7X7

We considered results with P values less than 5% to be statistically significant. All analysis was done with SPSS for Windows 10.0 statistical software.

RESULTS

The total mean score for acute histological changes was 2.11 (range, 0.02 to 0.56), and for chronic histological changes it was 4.09 (range, 0.14 to 0.76) (Table 2). The acute or chronic compromise of axial interstitium and airways characterized respectively acute and chronic bronchiolitis (Figure 4A). Similarly, the acute or chronic compromise of septal and peripheral interstitium, alveolar spaces, and vessels comprised the histologic pattern of chronic interstitial pneumonia (Figure 4B), diffuse alveolar damage (Figure 4C), and vasculitis (Figure 4D), respectively (Table 2). Table 3 shows the predictive ability for survival of the clinical and histological variables evaluated using the logistic regression model. Statistically significant impact on survival was found for male gender (P = 0.03), diffuse alveolar damage (P = 0.001), and chronic histological changes (P = 0.0004). Thus, being male was associated with a lower risk (O.R. = 0.18; P=0.03) of dying than being female. Presence of acute histological changes, such as diffuse alveolar damage at biopsy, increased the risk of death 17.5 times, whereas the presence of chronic histological changes increased risk of death related 2.5 times. Although not statistically significant, patients with immunosuppression, arterial hypertension, and chronic cardiac failure presented an apparently greater risk of death. When this model was evaluated on the original data used for its development, 26 of 32 (81.3%) patients were correctly classified as nonsurvivors, and 25 of 31 (80.7%) patients as survivors. Overall, 81% of the cases were correctly classified.

Table 2.

Mean, maximum, and minimum values of the acute and chronic histological score obtained by semiquantitative assessment

Histological compartments  Temporal evolution  Mean  Score Minimum  Maximum  Histological changes 
Septal interstitium  acute  63  0.19  1.25  Diffuse alveolar damage 
  chronic  63  0.55  1.38   
Alveolar spaces  acute  63  0.56  1.20   
  chronic  63  0.36  1.13  Chronic interstitial pneumonia 
Peripheral interstitium  acute  63  0.31  1.67   
  chronic  63  0.76  2.50   
Axial interstitium  acute  63  0.08  0.60  Acute bronchiolitis 
  chronic  63  0.45  1.75   
Terminal bronchioles  acute  63  0.38  1.00   
  chronic  63  0.14  0.67  Chronic bronchiolitis 
Respiratory bronchioles  acute  63  0.37  1.00   
  chronic  63  0.26  1.00   
Pre-acinar arterioles  acute  63  0.12  0.43  Acute vasculitis 
  chronic  63  0.44  1.25   
Post-acinar arterioles  acute  63  0.08  0.67   
  chronic  63  0.40  1.33  Chronic vasculitis 
Veins and lymphatics  acute  63  0.02  0.50   
  chronic  63  0.73  2.25   
Figure 4.

Prototypical histopathological changes: A (HE, 200X): chronic bronchiolitis with squamous metaplasia; B (HE, 200X): non-specific interstitial pneumonia (cellular pattern); C (HE, 200X): diffuse alveolar damage; D (HE, 200X): chronic vasculitis

(0.16MB).
Table 3.

Evaluation of the risk of death using the scoring system on surgical lung biopsies by the multiple logistic regression model (chi-square = 32.9; P < 0.001)

Variable  β  SE  Wald  P  Exp(B)  95% CI for Exp(B)
            Lower  Upper 
Gender  -1.68  0.78  4.61  0.031  0.18  0.039  0.86 
Diffuse alveolar damage  2.83  0.86  10.78  0.001  17.05  3.13  92.74 
Chronic histological score  0.86  0.25  11.41  0.000  2.36  1.43  3.89 
Systemic arterial hypertension  2.34  1.27  3.35  0.067  10.39  0.84  127.32 
Cardiac chronic failure  0.41  2.37  0.03  0.862  1.50  0.01  159.53 
Diabetes mellitus  -1.24  1.86  0.44  0.506  0.28  0.01  11.26 
Immunosuppression  0.88  0.73  1.48  0.22  2.43  0.58  10.19 
Constant  0.82  36.79  0.00  0.982       

β: coefficient of model; SE: Standard error; Wald: Wald statistics; P: probability of the null hypothesis; Exp (B): odds ratio; CI: confidence interval.

DISCUSSION

Diffuse infiltrates are usually a diagnostic challenge; they are also the most severe pulmonary nosologic pattern when compared to focal and nodular ones.13 At the timing of writing, the role of surgical lung biopsies in the management of diffuse pulmonary infiltrates remains obscure. Although such biopsies reveal some clinical homogeneity, diffuse pulmonary infiltrates can originate from different etiologies such as infectious pneumonias, organizing pneumonia, acute eosinophilic pneumonia, and pulmonary capillaritis, which thus require different treatment strategies.14

Several studies have been published concerning different aspects of surgical lung biopsies in distinct populations with diffuse infiltrates.15,16 Clinical implications of these biopsies have been greatly exploited, mostly concerning their contribution to the determination of prognosis through therapeutic changes, but also because such surgical biopsied can be carried out with relatively low morbidity and frequently promote changes in treatment.17–20

Clearly, most of the studies concerning surgical lung biopsies take into account only diagnostic information provided by routine histological analysis, usually regarded as the gold standard for clinical hypotheses in diffuse infiltrates,21 in addition to clinical data. Histopathological data from surgical lung biopsies have rarely been exploited in detail.22 The likely reason why such biopsies frequently fail to provide information in routine use is that histopathological details have not so far been adequately correlated with either routine clinical or pathological analyses. Frequently, clinical or radiological findings reflect such minimal tissue changes that they can be result in misdiagnosis. The question of interest is whether additional, more technologically enhanced information gathered from surgical lung biopsies or from clinical records can help us to better predict a patient’s outcome. Lung pathology undoubtedly comprises a series of complex stereotyped reactions, which make differential diagnosis using only qualitative approaches difficult. However, semiquantitative assessment is thought to be useful because it facilitates the creation of mathematical models to predict outcome. In a variety of conditions, especially diffuse pulmonary parenchymal diseases, a scoring system for quantitative assessment has been associated with guidance or evaluation of therapy response and prognosis.6–8 Thus, for all these reasons, we should not be surprised to learn that detailed pulmonary analysis of the different histological compartments, where alterations are classified in accordance with their acute or chronic character and semiquantified through a system of scores, can provide a significant prognostic contribution.

In addition to presenting a scoring system, our purpose included the correlation of histopathological findings of data concerning survival and epidemiological parameters. Descriptive analyses helped in selecting useful information for which statistical significance was verified through multiple logistic regression.

Most of our diagnoses included airway diseases in the same proportion as interstitial lung diseases; other studies found a higher percentage of idiopathic pulmonary fibrosis.13,16,23–25

We found a negative influence of diffuse alveolar damage and respiratory failure, mainly for men and with underlying disease (P > 0.05). It is widely known that the presence of underlying disease has a deleterious influence on the outcome of a pneumopathy and that diffuse alveolar damage is related to critical clinical pictures. Nevertheless, our study provided important quantitative information concerning these parameters, showing a 17 fold increase in risk of death in the presence of diffuse alveolar damage. Perhaps, according to the objective of this study, the most important evidence was the association of the chronic histological changes with survival. In fact, a direct association was found between low risk of dying and higher values of chronic histological changes. Our results confirm the prognostic importance of histopathological evaluation of surgical lung biopsies. This is possibly the first study concerning such biopsies with emphasis on detailed histological findings. Although further studies are required, our results suggest that quantitative assessment accomplished through a scoring system provides more prognostic information than does the routine clinical and pathological approach.

In conclusion, the detailed histological analysis of surgical lung biopsy specimens can provide more than nosological diagnosis; this approach can bring valuable information concerning prognosis. Additional study in a randomized and prospective trial could confirm this conclusion. We also believe that it is important to validate our semiquantitative assessment using a scoring system, as well as to extend it to other histological types of diffuse pulmonary disease, by studying the scoring system in additional patients.

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