athology and Pathophysiology of Chronic Obstructive Pulmonary Disease
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1 P REVIEW ARTICLE athology and Pathophysiology of Chronic Obstructive Pulmonary Disease Atsushi Nagai Abstract A variety of pathological changes have been observed in the central airways, peripheral airways and lung parenchyma of patients with chronic obstructive pulmonary disease (COPD). The characteristic changes in the central airways include inflammatory cellular infiltration into the airway wall and mucous gland enlargement. In the peripheral airways, various morphological changes are observed, including mucous plugging, epithelial abnormalities, inflammatory cellular infiltrates, fibrosis and distortion ; these changes lead to airway narrowing. In the lung parenchyma, emphysema defined as alveolar destruction and airspace enlargement is present. Although the major sites of airflow limitation in patients with COPD are most likely the peripheral airways, lesions in both the peripheral airways and the lung parenchyma contribute to chronic air flow limitations. (Internal Medicine 41: , 2002) Key words: chronic bronchitis, emphysema, bronchial asthma, airflow limitation, bronchiolitis, inflammation Introduction Chronic obstructive pulmonary disease (COPD) is a leading cause of morbidity and mortality throughout the world ( 1 ). Although the precise prevalence of COPD is unknown, the number of patients suffering from this disease is increasing. In addition, the development of COPD is related to a past history of cigarette smoking (2-6). The definition of COPD is based on functional abnormalities. Most previous definitions have characterized the disease as a respiratory condition in which the patient's airflow is limited as a result of chronic bronchitis and/or emphysema (7, 8). However, the Global Initiative for Chronic Obstructive Lung Disease (GOLD) very recently published a NHLBI/WHO workshop report in which COPD was defined as a disease state that is characterized by a limited airflow and that is not fully reversible (1). Airflow limitations are usually both progressive and associated with an abnormal inflammatory response of the lungs to noxious particles or gases. This workshop report states that chronic bronchitis and emphysema are no longer included in the definition of COPD because the former disease is of minor importance in calculating the impact of airflow limitations on the morbidity and mortality rates for COPD and the latter disease is a pathological term. This definition reflects the current knowledge of the pathology and pathophysiology of COPD. entral airways Pathology Patients with COPD exhibit enlarged bronchial mucous glands and an increased number of goblet cells (9-1 1) (Figs. 1, 2). These morphological changes may lead to mucus hypersecretion, although an increase in the number of goblet cells has not been consistently observed (12-14). The accepted definition of chronic bronchitis is chronic or recurrent excess secretion of mucous into the bronchial tree. Since the main source of bronchial mucous was thought to be the submucosal glands, the enlargement of these glands was considered to be a histological hallmark of chronic bronchitis. The degree of mucous gland enlargement is measured as the ratio of the thickness of the bronchial mucous glands to the thickness of the bronchial wall; this ratio is referred to as the Reid index (13). An earlier study reported a significant difference in the Reid index value for patients with chronic bronchitis ( ) and nonbronchitic patients ( ). The index was thus thought to be a useful diagnostic tool. However, subsequent works have shown considerable overlap between the Reid index frequency distributions for patients with chronic bronchitis and onbronchitic patients ( 15). Recent developments in bronchoscopy have enabled inflamed central airways to be more closely observed. Consequently, predominant inflammatory cellular infiltrations in the subepithelial region of the bronchial wall have been identified as activated CD8+ T-lymphocytes and macrophages (16). A number of neutrophils have been found in the bronchial lumen, and some neutrophil infiltrates have been identified near bronchial epithelium and submucosal glands (17). When exac- From the First Department of Medicine, Tokyo Women's Medical University, Tokyo Reprint requests should be addressed to Dr. Atsushi Nagai, the First Department of Medicine, Tokyo Women's Medical University, 8-1 Kawadacho, Shinju-ku, Tokyo Internal Medicine Vol. 41, No. 4 (April 2002) 265
2 Nagai Figure 2. Scanning electron micrograph showing secretion mucous (arrow) from increased goblet cells (x6,000). of Figure 1. The mucous glands of a patient with COPD form a much higher proportion of the bronchial wall (HE stain, xl50). erbated, the number of eosinophils lial region increases (1 8). the subepithe- airways P The peripheral airways are considered to be the major sites of increased airway resistance in patients with COPD (19). Various structural changes can be observed in these regions, including goblet cell metaplasia, squamous metaplasia, inflammatory cellular infiltrations, an increased amount of smooth muscle, fibrosis and pigmentation (19-24). Mucous plugging is also frequently observed in the airway lumen. These pathological changes may lead to an increase in airway wall thickness and the subsequent narrowing of the airway lumen (Fig. 3)(25). Knowledge of how inflammation leads to structural changes is important for an understanding of the relationship between pathological changes and the severity of air flow limitation. Inflammation appears to be the earliest stage of lesion formation and, by itself, can cause mild chronic airflow limitations (26). Fibrosis and goblet cell metaplasia are thought to follow nflammation (27) and cause irreversible airflow limitations. i Recent studies focusing on the nature of the inflammatory 266 Figure 3. Light micrograph of lung parenchyma region in a patient with severe COPD. The narrowed lumens in the airways and vessels are observed in the emphysematous lesions (HE stain, x8). cells have identified the infiltration of CD8+ T-lymphocytes into the walls of the peripheral and central airways (16, 28). These findings suggest that a similar inflammatory process occurs in both types of airways in COPD patients. The peripheral airways are infiltrated by a number of macrophages that re recruited via transforming growth factor-p l (29). On the basis of morphologic studies, the loss of alveolar attachments (radial traction) around bronchioles has been proposed as the mechanism responsible for chronic airflow obstruction (30, 3 1). Airway narrowing and bronchiolar deformi- ties have been associated with a loss of alveolar attachment (3 1-33), and a significant relationship between the loss of normal attachments and the severity of emphysema has been idena eripheral infiltrating Internal Medicine Vol. 41, No. 4 (April 2002)
3 p Pathology and Pathophysiology of COPD tified (33). L ung parenchyma In patients with emphysema, the lung parenchyma is characterized by an enlargement of the air spaces accompanied by alveolar destruction. Conventionally, three types of emphysema have been described: centriacinar emphysema, panacinar emphysema and distal acinar emphysema. As distal acinar emphysema is not associated with air flow limitations, only centriacinar and panacinar emphysema will be described here. Centriacinar emphysema is characterized by alveolar destruction in the respiratory bronchioles in the central area of the acinus. These lesions are predominantly found in the upper lobes of smokers. Panacinar emphysema involves the dilatation of the entire acinus, with the lower lobe dilated to a larger degree than the upper lobe, deficiency of al -antitrypsin and an early onset are associated with panacinar emphysema. Both types of emphysema are characterized by alveolar destruction with loss of the capillary bed. The mechanism responsible for the development of emphysematous lesions is thought to be an imbalance in protease and antiprotease enzymes in the lung. Oxidative stress has also been proposed as a potential mechanism (34), although this hypothesis has yet to be proven. Inflammation is assumed to cause the characteristic alveolar destruction seen in emphysematous lesions. Both neutrophils and macrophages play an important role in increasing protease activity in the lung. However, there was no difference between the upper and lower lobes in the numbers and types of inflammatory cells, whereas the severity of the emphysematous lesions is more extreme in the upper lobe (35, 36). Recently, the predominance of T-lymphocytes in emphysematous lungs has been reported. One study described a significant association between alveolar wall destruction and the number of CD8+ T-lymphocytes (37). However, our data using specimens obtained from lung volume reduction surgery have shown a relationship between the number of CD4+ T- lymphocytes and alveolar wall destruction (unpublished observation) (Fig. 4). Further study is necessary to determine the recise role of T-lymphocytes in alveolar destruction. In summary, lesions develop when central airways are irritated and respond with mucus hypersecretion and mucous gland enlargement. The peripheral airways respond by becoming inflamed, leading to fibrosis and airway narrowing. In the parenchyma, the inflammation results in alveolar wall destruction and emphysema. Pathophysiology Most patients with chronic airflow limitations have central airway lesions, peripheral airway lesions, and emphysema in varying combinations of severity. Many reports have described the presence of peripheral airway lesions in patients with severe chronic airflow limitations. However, the great majority of these reports describe the patients as having either emphysema or chronic bronchitis; assessing the functional significance of individual morphological abnormalities is thus difficult. To clarify the relative importance of central airway lesions, peripheral airway lesions, and emphysema in expiratory airflow abnormalities, quantitative functional-structural correlaive studies have been performed. The clinico-pathological correlative studies showed that peripheral airway lesions resulting in airway narrowing play a significant role in causing airflow limitation. Emphysematous lesions were also found to limit expiratory airflow. The largest study, involving a wide range of airflow limitations, indicated that in patients with moderate to severe emphysema, the loss of elastic recoil induced by the emphysematous lungs has a stronger effect on airflow limitation than that of the peripheral Figure 4. Morphometric study shows the relationship between the number of CD4+ T-lymphocytes and the extent of emphysema by the lower volume density of the lung parenchyma (Vvalv). Internal Medicine Vol. 41, No. 4 (April 2002) 267
4 Nagai Figure 5. Scanning electron micrograph shows that the loss of alveolar attachments around peripheral airways contributes to the narrowing of the lumen in the peripheral airways (x38). Figure 6. The prevalence of grossly visible emphysema increases as FEV1 declines. lesions (24). When the emphysema is mild, however, the peripheral lesions are most likely the primary cause of the airlow limitation. The loss of alveolar attachments around peripheral airways can contribute to the narrowing of the lumen in the peripheral airways, leading to airflow limitation (Fig. 5) (38). This effect may occur as a result of emphysema, since the loss of alveolar attachments reflects the severity of emphysema which in turn is related to airflow limitation. A recent study using computed tomography of the chest to assess emphysema clearly showed that the prevalence of grossly visible emphysema increases as FEV1 declines (Fig. 6), although the authors concluded that irflow limitations and emphysema were not related (39). In summary, functional-morphologic correlative studies involving quantitative assessments of the airways and lung parenchyma have indicated that emphysema may be the most significant factor in cases of moderate and severe chronic airflow limitation; peripheral airway lesions also cause airflow limitation, but these lesions are likely to play a secondary role in the case of serious COPD. In addition, central airway lesions are probably not very important in airflow limitation. Concomitant lesions in the peripheral airways and lung parenchyma are thus responsible for chronic airflow limitations in the peripheral airway regions. References 1 ) NHLBI/WHO workshop report. Global initiative for chronic obstructive lung disease. National Institutes of Health, National Heart, Lung, and Blood Institute, Publication No. 2701, April, ) U.S. Surgeon General. The Health Consequences of Smoking: Chronic obstructive lung disease. U.S. Department of Health and HumanServices, Washington, D.C. DHHS Publication No , ) Fletcher C, Peto R. The natural history of chronic airflow obstruction. Br Med J l: , ) Burrows B, Knudson RJ, Cline MG, Lebowitz MD. Quantitative relationships between cigarette smoking and ventilatory function. AmRev Respir Dis 115: , ) Auerbach O, Hammond EC, Garfinkel L, Benante C. Relation of smoking and age to emphysema. Whole-lung section study. N Engl J Med 286: , ) Higgins MW,Keller JB, Becker M et al. An index of risk for obstructive airways disease. AmRev Respir Dis 125: , ) American Thoracic Society. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. AmJ Respir Crit Care Med l52: S77-S120, ) Siafakas NM, Vermeire P, Pride NB, et al. and The European Respiratory Society Task Force. Optimal assessment and management of chronic obstructive pulmonary disease (COPD). Eur Respir J 8: , ) Reid L. Pathology of chronic bronchitis. Lancet 1: , ) Jamal K, Cooney TP, Fleetham JA, Thurlbeck WM.Chronic bronchitis. Correlation of morphologic findings to sputum production and flow rates. Am^RevRespir Dis 129: , ) Nagai A, West WW,Paul JL, Thurlbeck WM.The National Institutes of Health Intermittent Positive-pressure Breathing Trial : Pathology studies. I. Interrelationship between morphologic lesions. AmRev Respir Dis 132: , ) Niewoehner DE, Kleinerman J, Knoke JD. Regional chronic bronchitis. AmRev Respir Dis 105: , ) Reid L. Measurement of the bronchial mucous gland layer: a diagnostic yardstick in chronic bronchitis. Thorax 15: , ) Mullen JB, Wright JL, Wiggs BR, Pare PD, Hogg JC. Reassessment of inflammation of airways in chronic bronchitis. Br Med J 291: , ) Thurlbeck WM.Aspects of chronic airflow obstruction. Chest 72: , ) O'Shaughnessy TC, Ansari TW, Barnes NC, Jeffery PK. Inflammation in bronchial biopsies of subjects with chronic bronchitis: inverse relationship of CD8+ T lymphocytes with FEV1. AmJ Respir Crit Care Med 155: , ) Saetta M, Turato G, Facchini FM, et al. Inflammatory cells in the bronchial glands of smokers with chronic bronchitis. AmJ Respir Crit Care Med 156: , ) Saetta M, Di Stefano A, Maestrelli P, et al. Airway eosinophilia in chronic bronchitis during exacerbations. AmJ Respir Crit Care Med 150: , 19) Hogg JC, Macklem PT, Thurlbeck WM. Site and nature of airway ob-, 268 InternalMedicine Vol. 41 No. 4 (April 2002)
5 3 3 Pathology and Pathophysiology of COPD struction in chronic obstructive lung disease. N Engl J Med 278: , ) Niewoehner DE, Kleinerman J, Rice DP. Pathologic changes in the peripheral airways of young cigarette smokers. N Engl J Med 291: , ) Cosio MG, Hale KA, Niewoehner DE. Morphologic and morphometric effects of prolonged cigarette smoking on the small airways. Am Rev Respir Dis 122: , ) Wright JL, Lawson LM, Pare PD, Kennedy S, Wiggs B, Hogg JC. The detection of small airways disease. Am Rev Respir Dis 129: , ) Mitchell RS, Stan ford RE, Johnson JM, Silvers GW, Dart G, George MS. The morphologic features of the bronchi, bronchioles and alveoli in chronic airway obstruction: A clinicopathological study. Am Rev Respir Dis 114: , ) Nagai A, West WW,Thurlbeck WM.The National Institutes of Health Intermittent Positive-pressure Breathing Trial: Pathology studies. II Correlation between morphologic findings, clinical findings, and evidence of expiratory airflow obstruction. AmRev Respir Dis 132: , ) Nagai A, Yamawaki I, Thurlbeck WM,Takizawa T. Assessment of lung parenchymal destruction by using routine histologic tissue sections. Am Rev Respir Dis 139: , ) Cosio MG, Ghezzo H, Hogg JC, et al. The relations between structural changes in small airways and pulmonary function tests. N Engl J Med 298: , ) Hogg JC, Cosio M. The Pathophysiology of Small Airways, in: Sadoul P, Milic-Emili J, Simonsson BG, Clark TJH, Eds. Small Airways in Health and Disease. Excerpta Medica, New York, 1979: ) Saetta M, Di Stefano A, Turato G, et al. CD8+ T lymphocytes in the peripheral airways of smokers with chronic obstructive pulmonary disease. AmJ Respir Crit Care Med 157: , ) de Boer WI, van Schadewijk A, Sont JK, et al. Transforming growth factor beta 1 and recruitment of macrophages and mast cells in airways in chronic obstructive pulmonary disease. AmJ Respir Crit Care Med 158: , ) Pratt PC, Haque A, Klugh GA. Correlation of postmortem function and structure in normal and emphysematous lungs. AmRev Respir Dis 83: , j 1) Anderson AE, Foraker AG. Relative dimensions of bronchioles and parenchymal spaces in lungs from normal subjects and emphysematous patients. AmJ Med 32: , ) Linhartova A, Anderson AE, Foraker AG. Further observation on luminal deformity and stenosis of non-respiratory bronchioles in pulmonary emphysema. Thorax 32: 53-59, ) Nagai A, Yamawaki I, Takizawa T, Thurlbeck WM.Alveolar attachment^ in emphysema of human lungs. AmRev Respir Dis 144: , ) Repine JE, Bast A, Lankhorst I, and Oxidative Stress Study Group. Oxidative stress in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 156: , ) Wright JL. Airway inflammatory cells in upper and lower lobes in lungs of patients with and without emphysema. Pathol Res Pract 183: , ) Wright JL, Wiggs BJ, Hogg JC. Airway disease in upper and lower lobes in lungs of patients with and without emphysema. Thorax 39: , ) Saetta M, Baraldo S, Corbino L, et al. CD8+ve cells in the lungs of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 160: , ) Nagai A, Thurlbeck WM.Scanning electron microscopic observations of emphysema in humans. AmRev Respir Dis 144: , ) Hogg JC, Wright JL, Wiggs BR, Coxson HO, Saez AO, Pare PD. Lung structure and function in cigarette smokers. Thorax 49: , Internal Medicine Vol. 41, No. 4 (April 2002) 269
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