C a r d i o p u l m o n a r y I m a g i n g • R ev i ew

Arakawa and Honma Imaging of Honeycomb Lung Cardiopulmonary Imaging Review

Honeycomb Lung: History and Current Concepts
Hiroaki Arakawa1 Koichi Honma2
Arakawa H, Honma K

OBJECTIVE. Originally used to describe the macroscopic appearance of various pathologic processes with multiple cysts, honeycomb lung is now the term used to describe endstage pulmonary fibrosis. The purpose of this article is to discuss the history and imaging of honeycomb lung. CONCLUSION. Honeycomb lung is considered one of the important CT findings in usual interstitial pneumonia. An additional challenge for radiologists is that different pathologic processes can mimic honeycomb lung. Therefore, a precise understanding of honeycomb lung is necessary.

Keywords: CT, honeycomb lung, idiopathic interstitial pneumonia, interstitial lung disease DOI:10.2214/AJR.10.4873 Received April 29, 2010; accepted after revision August 28, 2010.
1 Department of Radiology, Dokkyo Medical University, 880 Kita-Kobayashi, Mibu, Tochigi, 3210293 Japan. Address correspondence to H. Arakawa (arakawa@dokkyomed.ac.jp). 2 Department of Cancer Center Pathology, Dokkyo Medical University, Tochigi, Japan.

AJR 2011; 196:773–782 0361–803X/11/1964–773 © American Roentgen Ray Society

he term “honeycomb lung” originated in the 19th century in Germany where medicine was highly developed in that era. We can go back as far as 1858 when Kessler described a case of congenital bronchiectasis [1]. Since then, the honeycomb appearance of the lung was named, variously by different authors, Wabenlunge (honeycomb lung), Zystenlunge (cystic lung), Schwammlunge (spongy lung), and Sacklunge (sacculated lung) [1, 2]. In the German literature, honeycomb lung was usually considered a congenital malformation or anomalous development of the lung with bronchiectasis [2] (Fig. 1). It seems that the term “honeycomb lung” was not applied to chronic interstitial pneumonia in Germany. In the first half of the 20th century, the idea of idiopathic pulmonary fibrosis (IPF) was not yet established, and only occasional case reports were found, in which the authors called their cases different names or only reported the clinical and pathologic findings [3–6]. The famous report by Hamman and Rich [3], which initially appeared in 1935, did not use the term “honeycomb lung.” In the subsequent English literature, cases of presumed IPF were reported under the name bronchiolar emphysema [5], pulmonary muscular hyperplasia [4], or cystic pulmonary cirrhosis [6]. Originating in the German literature, these names were translated into English and were discussed as a rare and new disease entity [7, 8]. Sibert and Fisher

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[5], who used the term “bronchiolar emphysema,” considered their cases to be a special type of pulmonary emphysema. The term “honeycomb lung” first appeared in the English literature in 1949 in a study by Oswald and Parkinson [9]. Sixteen clinical cases of honeycomb lung were presented in detail. The cases included, as interpreted by current medical knowledge, Langerhans cell histiocytosis, lymphangioleiomyomatosis (LAM), and probable chronic interstitial pneumonia, which was not a disease diagnosed in that era [9] (Fig. 2). In the definition by Oswald and Pakinson, honeycomb lung was “descriptive of the appearance of the cut surface of the lungs” as being “thin-walled cysts distributed uniformly throughout the substance of both lungs, varying in sizes up to a maximum of 1 cm in diameter.” A more comprehensive report with a pathologic description followed in 1956 by Heppleston [10], who in his practice dealt with a wide variety of diseases and clinical backgrounds (32 patients were coal workers). In this report, most cases were probable chronic interstitial pneumonia, which also included a small number of those with sarcoidosis, berylliosis, eosinophilic granuloma, LAM, giant cell interstitial pneumonia, scleroderma, and even tuberculous bronchopneumonia. Thus, before the 1960s, honeycomb lung was considered the macroscopic appearance of lung diseases comprising various histopathologic processes and causes, partly because physicians had little idea of identify-

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B. which are mostly discrete and not subpleural. which forms the honeycomb appearance [10].Arakawa and Honma Fig. A. lower lobe. A. There are multiple thin-walled cysts occupying most of lobe. B.” Pathologic Description In the initial detailed description of honeycomb lung. (Elastica-Goldner stain) B 774 AJR:196. Photograph shows macroscopic appearance of surgically resected right lower lobe. simulating honeycomb lung. A Fig. although some cysts are clustered. 2—24-year-old woman with lymphanigoleiomyomatosis (LAM). Thin-section CT image at level of tracheal carina shows multiple thin-wall cysts. Fibrosis is limited to area of cyst wall (arrows ) and it is obvious that cysts are not result of end-stage pulmonary fibrosis. irrespective of the cause. Thin-section CT image shows extensive bronchiectasis involving whole right. Photomicrograph of surgically resected lung tissue reveals clusters of thin-walled cysts in subpleural area. It was not until 1965 that honeycomb lung was limited to chronic interstitial pneumonia when Meyer and Liebow [11] suggested honeycombing as “the end-stage of chronic interstitial pneumonia no matter what the etiology. Appearance was called “Wabenlunge ” in Germany in late 19th and early 20th centuries. A ing the diseases in the way we do now and partly because of the macroscopic similarity of various cystic lung diseases. These changes were the consistent pathologic finding of honeycomb lung. Note that cysts are lined along bronchial tree. Appearance is not typical of honeycomb lung by current definition. Note that some cysts contain mucous material (arrows). April 2011 . Heppleston [10] stated that the es- B sential change is the obliteration of bronchioles by fibrosis or granulomata and compensatory dilatation of neighboring bronchioles. 1— 57-year-old woman with bronchiectasis.

with relatively uniformly sized cysts…that A Fig. These features are different from honeycomb lung. The other bronchioles showed abnormal changes in direction. in which the pathologic definition of honeycomb lung follows that of Genereux [16] as “destroyed and fibrotic lung tissue containing numerous cystic airspaces with thick fibrous walls. various lung diseases can result in end-stage lung (honeycomb lung). B. bronchiolectasis. dermatomyositis. eosinophilic granuloma. Genereux [16] discussed honeycomb lung from the standpoint of the end stage of interstitial lung disease of various causes. April 2011 775 . and there were anastomoses between anatomically independent bronchioles. when the macroscopic appearance of the lung was imaged imprecisely and thus had substantial limitations. defined by “visualization of multiple lucent shadows from 2 to 10 mm in size” on a chest radiograph. B (Fig. and sarcoidosis in addition to idiopathic pulmonary fibrosis (HammanRich) as the common lung diseases in their gamut of honeycomb lung. This idea coincides with that of Meyer and Liebow [11]. Therefore. These ectatic bronchi simulate appearance of honeycombing. Honeycomb lung. A. In the 1970s. the concept gradually changed. especially the terminal and respiratory bronchioles. 3— 62-year-old man with fibrotic nonspecific interstitial pneumonia (NSIP). 4 continues on next page) AJR:196.” Significantly. representing the late stage of various lung diseases. Initial thin-section CT image reveals multiple clustered cysts of up to 10 mm in lower lobes. However. which were displayed in three dimensions through photographic reconstruction [12]. The radiologic concept changed later than the pathologic one. branching pattern. Katzenstein [18] stated that honeycomb lung “has a characteristic gross appearance. tuberculosis. Fig. Thin-section CT image reveals mixture of consolidation and ground-glass opacity with traction bronchiectasis (arrows ). Lung tissue intervenes between ectatic bronchi and cystic spaces are not clustered. Recent Definition of Honeycomb Lung Pathology The Fleischner Society has recently revised its glossary terms. with complete loss of acinar architecture” [17]. honeycomb lung in scleroderma.Imaging of Honeycomb Lung In another study. they can be tracked back to bronchial tree with accompanying pulmonary artery on contiguous images. pneumoconiosis. Radiologic Description The early radiologic description of honeycomb lung also indicated the various causes and pathophysiology [13]. which is “characterized by cystic spaces of variable size and extent and is caused by alveolar septal dissolution. and abrupt amputation. sarcoidosis. lipoid pneumonia. 4—78-year-old woman with idiopathic pulmonary fibrosis (IPF). However. which causes the bronchioles to dilate or amputate. and IPF was studied by continuous sections of three resected lungs and eight autopsy lungs. and obstructive emphysema. Follow-up thin-section CT image obtained 15 months later shows obvious enlargement of each cyst. these descriptions were in the era of the chest radiograph. Reed and Reeder [14] listed cystic bronchiectasis. included not only diffuse interstitial fibrosis but also bronchiectasis and even bullous emphysema [13]. These authors insisted that the primary abnormality of honeycomb lung is the fibrous or granulomatous process of alveoli and ducts. Langerhans cell histiocytosis. who believed that the lung can respond only in a stereotyped manner to a variety of insults. Felson [15] emphasized interstitial fibrosis as the basis of honeycomb lung and excluded cystic bronchiectasis and bullous emphysema from its definition. largest reaching 20 mm. The authors found that the pathologic process in the honeycomb area was independent of the original disease and was fundamentally diffuse saccular or cystic bronchiolectasis involving the whole lobule.

E. whereas others just look emphysematous. D. 5— 45-year-old woman with Langerhans cell histiocytosis. (H and E) E Fig. Note presence of bronchial epithelization of some of cysts (arrow ). Thin-section CT image shows discrete cystic spaces in center of right upper lobe. which is different from typical honeycomb cyst in usual interstitial pneumonia (UIP). Photograph of lungs obtained at autopsy performed 2 months after B shows cobblestone appearance of lung surface. April 2011 . Photomicrograph at area of honeycomb lung shows multiple cysts with different sizes in background of dense fibrous scar. Most cysts spare subpleural area and are predominant in upper lobes. C. Some cysts are thin-walled. Photograph of coronal cut surface of resected lungs shows honeycomb lungs.Arakawa and Honma C D Fig. 4 (continued)—78-year-old woman with idiopathic pulmonary fibrosis (IPF). closely resembling CT appearance. 776 AJR:196.

A. Pathologically. On thin-section CT images.Imaging of Honeycomb Lung are set in a background of dense scarring” and “microscopically…honeycomb lung is characterized by enlarged airspaces surrounded by fibrosis and lined by bronchiolar or hyperplastic alveolar epithelium. Some researchers use the term “microscopic honeycombing” to describe 1to 2-mm dilated bronchioles surrounded by airless fibrotic lung on a pathologic specimen [20]. Churg [19] described honeycomb lung as “a variable combination of thick-walled cysts…. 18].” which indicates a rather nonspecific pathologic condition [19]. who developed squamous cell carcinoma. stated that honeycomb lung is “a number of closely approximated ring shadows Fig. Cystic spaces are confluent and are larger with thinner walls than those of honeycomb lung. honeycomb lung is nonspecific as to cause. Photomicrograph of cystic space shows destruction and fibrosis of pulmonary parenchyma. the area corresponds to markedly increased lung attenuation with dilated bronchioles and is therefore different from the macroscopic honeycomb lung. asbestosis. “In addition to specific diffuse diseases. which was published in 1984.” so they are macroscopically identifiable [17]. Whether the pathologic process that occurs in the “microscopic honeycombing” has a similar clinical and pathophysiologic significance to that of (macroscopic) honeycomb lung is still to be determined. the Fleischner Society definition indicates. which is compatible with interstitial fibrosis. interstitial granulomatous diseases. In another pathology book. which can image the lungs close to their macroscopic appearance [21]. Radiology A recent definition of honeycomb lung in radiology is based on thin-section CT. which corresponds to the previous understanding [11.” According to Katzenstein. April 2011 777 . (H and E) D. 6— 68-year-old man with combined emphysema and chronic interstitial pneumonia. This is considered coexistence of emphysema and chronic interstitial pneumonia and not honeycomb lung. indicating presence of chronic interstitial pneumonia. The combination of parenchymal collapse…and collagen deposition accounts for the major manifestation of this lesion. (Elastica-Goldner stain) A B C D AJR:196. B. Thin-section CT image of lung tumor reveals multiple thin-walled cysts and emphysema. with varying-sized cyst. Groundglass opacity is noted adjacent to cystic area (arrows ). which is separated from normal lung by interlobular septa (asterisks ). “the cysts range in size from a few millimeters to several centimeters in diameter.” He continued. diffuse alveolar damage. The initial definition by the Fleischner Society. and a diverse group of diseases can lead to honeycombing (idiopathic interstitial pneumonia [IIP]. Photograph of cut surface (corresponding to CT slice) of surgically resected left lower lobe shows multiple cysts of various sizes. which may range from a few millimeters to a few centimeters in diameter. localized scars of many causes can appear as honeycombed lung. C. giving appearance of honeycombing. and intervening solid fibrous tissue. Photomicrograph shows presence of fibroblastic foci (arrow ). and eosinophilic granuloma).

which challenges radiologists in CT diagnosis. This appearance mimics honeycomb lung. However. In two autopsy series of patients with honeycombing of UIP.1 years) [30]. “the cystic air spaces of honeycomb lung tend to share walls” [24]. However. and shows far worse prognosis than other chronic interstitial pneumonia [26]. With the common use of CT examinations in this era of MDCT. Thin-section CT image obtained 5 years later shows cluster of multiple cysts in area of previous emphysema. the progression of honeycomb lung ranged from 0% to 11% of the lungs per month (median. less frequently. usually of comparable diameters on the order of 0. it can also occur in a minority of patients with acute interstitial pneumonia and diffuse alveolar damage [31. 3. but it can occur as early as 1 week after the onset of symptoms [31]. This emphasis originated from the recent consensus statement about idiopathic pulmonary fibrosis published in 2000 by American Thoracic Society and European Respiratory Society. The large 778 AJR:196. “Clustered cystic air space. IPF is a progressive disease. 3). patients underwent paired inspiratory and expiratory volume scanning of the lung.5 cm… usually subpleural and characterized by welldefined walls” [17]. Thin-section CT image shows emphysema in periphery of right lower lobe. Progression of Honeycomb Lung Because honeycomb lung is the end stage of interstitial pneumonia.3–1. the earliest abnormality was faint ground-glass opacity or. honeycomb lung is preceded by the presence of patchy ground-glass opacity and reticulation within a secondary lobule [29]. The size and wall thickness of the cysts vary among the authors who use the term. are almost the same except for the size and location. which were in the era of the chest radiograph in the first version and of CT in the second version. said. stenosis or abrupt angulations of bronchiole and slitlike structures between the cysts and bronchioles were found. the prognosis is still regarded as poor [28]. This means that traction bronchiolectasis with intervening lung should not be called honeycombing (Fig. 33] (Fig. which is in concert with the statement by Meyer and Liebow [11] and Genereux [16]. 32].Arakawa and Honma Fig. There is minimum increase in lung attenuation associated with emphysematous area. In a series of 29 IPF patients. honeycomb lung is defined as “clustered cystic air spaces. diagnosis should be performed with thin-section CT [25]. typically of comparable diameters on the order of 3–10 mm but occasionally as large as 2. This disease is progressive by the day or week. which emphasized the clinical relevance of discriminating UIP from other IIP [25]. 30].4%) and was fastest in the lower lobes [29]. A representing air spaces 5–10 mm in diameter with walls 2–3 mm thick…whose occurrence implies end-stage lung” [22]. A. The speed of progression of honeycomb lung is poorly understood. It is presumed that a long asymptomatic period exists before honeycomb lung develops and the patient becomes symptomatic. and the size of honeycomb cysts was evaluated using multiplanar reformation [34].5 cm. Although most cases of honeycomb lung are seen in chronic lung disease. These earlier definitions. there must be an abnormality that precedes it. Honeycomb lung is not the initial feature. Because of the small size of the cyst. However. normal or near-normal lung progressed to honeycomb lung within a median of 12. 7— 56-year-old man with emphysema who developed interstitial pneumonia during follow-up. Among idiopathic interstitial pneumonia.0 cm but as much as 2. The size of the honeycomb cyst usually increases during follow-up [33]. it is not end-stage of chronic fibrosing interstitial pneumonia but superimposition of groundglass opacity on emphysema.1 years (range. April 2011 . often with acute exacerbation. B. which were regarded as the causes of progressive enlargement of honeycomb cysts [12. Although a new antifibrotic drug has emerged as a possible treatment option for IPF [27].” and thus “the term should be used with care [because] it may directly impact patient care” [17]. B The latest definition emphasizes the importance of honeycombing as the diagnostic criterion of UIP. and the result is often fatal. The second statement by the Fleischner Society. In another series of 14 patients with chronic interstitial pneumonia and silicosis observed for a median of 15. which are often thick—a CT feature of diffuse pulmonary fibrosis” [23]. In another study of 97 patients with end-stage lung disease. 0. In one report of 14 cases of silicosis that developed chronic interstitial pneumonia with honeycombing. which was published in 1996.7–19. In the latest version from the Fleischner Society. 4). Over time. In the case of UIP. The earliest CT abnormality of UIP is poorly understood. recent understanding indicates that “honeycombing is often considered specific for pulmonary fibrosis and is an important criterion in the diagnosis of usual interstitial pneumonia (UIP). coarse reticulation [30]. cases of IPF without honeycomb lung are expected to be increasingly found. this study was performed with 10-mm slice thickness.4 years. intralobular reticulation increases and traction bronchiolectasis gradually appears in the area of the ground-glass opacity while the ground-glass opacity diminishes and finally results in honeycombing [29. Although different disease processes result in the same pathologic and radiologic appearance. usually is subpleural and characterized by well-defined walls.

SD. Honeycomb lung in UIP is usually subpleural and is predominant in posterior and lower lobes [29. April 2011 779 . 4. honeycombing was identified in 41–100% of UIP. B. four silicosis. show honeycombing in 0–30% and 4. Nonspecific interstitial pneumonia (NSIP) and desquamative interstitial pneumonia (DIP). In acute interstitial pneumonia. although honeycombing is the common finding of UIP. Honeycomb Lung as the CT Criterion of UIP Honeycombing is often considered specific to pulmonary fibrosis and is an impor- tant criterion in the diagnosis of UIP [17]. 50]. Appearance is different from honeycomb lung in UIP.7 mm. the sensitivity and specificity of the presence of honeycombing in the diagnosis of UIP were 90% and 86%. eight Langerhans cell histiocytosis. whereas the small cysts (mean. however. This characteristic distribution distinguishes UIP from other diseases with honeycomb lung. nine sarcoidosis.6 mm. Pathologic diagnosis was also different from typical UIP pattern. Arrows indicate pleural surface. D. 10. SD. three LAM. one berylliosis. 20. 46–48]. 49]. (Elastic-Goldner stain) honeycomb cysts (mean. AJR:196. C. In a study of 61 various end-stage lung diseases (26 UIP. it is not the specific CT finding of UIP. 35. 32. which are the chronic interstitial pneumonias of IIP and are the im- portant differential diagnostic considerations.Imaging of Honeycomb Lung A B C D Fig. respectively [45]. Initial CT image shows slight increase in lung attenuation in both lung bases (arrows ). 38. CT finding is different from honeycomb lung of usual interstitial pneumonia (UIP).7 mm) tended to have thinner walls and did not communicate with the airways and thus did not change in size during forced exhalation. five asbestosis. giving appearance of emphysematous cysts (arrows ). ground-glass opacity is obvious and multiple lung cysts are identified in area of ground-glass opacity. 2. In CT image obtained 8 years later. CT image obtained 5 years after B shows further progression of ground-glass opacity and increased number and size of lung cysts. respectively [37. the frequency is lower. In one report of 168 cases of suspected IIP. Photomicrograph of lung specimen shows multiple lung cysts in area of interstitial fibrosis (arrowheads ). The data suggest that the progressive enlargement of honeycomb cysts is partly due to air trapping by the check-valve mechanism. ranging from 6% to 14% [31. A.3 mm) did have communication with the airways and their size changed on expiration [34]. By definition. four chronic hypersensitivity pneumonitis. These cysts are thin-walled and spare subpleural zone. although some cysts are clustered.3–39%. depending on the reported series [35–44]. In previous literature. 8— 64-year-old man with silicosis and chronic interstitial pneumonia.

the development of ground-glass opacity in the area of emphysema should not be called honeycomb lung. Pathologically. Although emphysema is pathologically defined as loss of lung parenchyma without fibrosis. Although the definition is straightforward. Located in the subpleural area. A and one talcosis). and is often clustered (Fig. the presence of this fibrosis can be a risk factor of acute exacerbation during cytotoxic drug treatment [59] and after pulmonary surgery [60]. it is important to use the term in consensus. 9— 62-year-old man with emphysema and chronic interstitial pneumonia. In the previous literature. Thus. its use is limited mostly to the end-stage lung with interstitial fibrosis. 6). although there seems to be no threshold that discriminates UIP from other IIP. In the meantime.3–3. emphysematous lung or cystic areas were misdiagnosed as honeycombing in three cases [47]. subpleural cysts or bulla. A. although there is typical honeycomb lung in the lower lobes. 7). 8). B. the extent of honeycomb cyst is another important consideration when diagnosing UIP. including bronchiectasis and congenital cystic lung disease. in a study of 314 cases B of IPF. The end result is similar to honeycomb lung. In a study of 34 patients with either UIP or NSIP and emphysema. which is one of the types of emphysema. which is often relatively thin walled and presents a diagnostic challenge to radiologists. the definition and clinical meaning of honeycomb lung have changed and may change from the present definition in the future. paraseptal emphysema. In addition to the distribution. 9). diagnosing honeycomb lung in IPF or UIP is sometimes not easy for radiologists. April 2011 . showing similarity of honeycomb cyst and paraseptal emphysema. might show a honeycomb appearance if the abnormality involves the emphysematous area and thus would likely be misdiagnosed as UIP [47]. Finally. both the frequency and extent are significantly higher in UIP than in DIP or NSIP. is located subpleurally. This variation could originate from the varied appearance of cystic structures in chronic interstitial pneumonia. One is the definition of the terminology and the others are associated with radiographic diagnosis with CT. 780 AJR:196. The problem of diagnosis originates from the historical change of the concept and the different circumstances in which it is made. Although such fibrosis may be different from UIP [58]. In these cases. NSIP and DIP. On the other hand. especially of the paraseptal type. 46–48]. with a high degree of confidence in 67% [51] (Fig. 38. honeycombing meant nonspecific cystic pulmonary conditions. Furthermore. all these structures appear cystic and often have walls. these different pathologic processes are often continuous with each other in the subpleural zone.31.21 to 0. and emphysema. However. the characteristic distribution of honeycombing made it possible to diagnose UIP in 88% of the cases. the extent of honeycombing in NSIP and DIP is reported as 0. However. The coexistence of emphysema is reported in the subset of patients with IPF. which indicates rather poor agreement [36]. which is rather a common phenomenon because both diseases are associated with cigarette smoking [53–56].7–10% of the lung parenchyma. It has been reported that the extent of honeycombing ranged from 3% to 21% of the lung parenchyma in UIP [35–44]. and when it is used. In these reports. in which there can be traction bronchiolectasis.Arakawa and Honma Fig. Emphysema and cystic spaces can be challenging in the presence of overlapping ground-glass opacity [47]. differentiating the two is almost impossible.7% and 0. has definite walls. emphysema and interstitial fibrosis develop and progress simultaneously in the same lung area [61] (Fig. Thus. paraseptal emphysema is often accompanied by fibrosis in its walls [62]. This situation can occur with pneumonia in emphysematous lung but more problematic is the development of chronic interstitial pneumonia in emphysematous lung during follow-up (Fig. interpreters should have a unanimous opinion and image of what is meant by honeycomb lung. Problems in Diagnosing Honeycomb Lung There are several difficulties in the diagnosis of honeycomb lung. It should be kept in mind that honeycomb lung is the end stage of pulmonary fibrosis. in the recent literature. Future of CT Diagnosis of Honeycomb Lung Because the term “honeycomb lung” is closely linked with the concept of the disease and with the classification of idiopathic interstitial pneumonia. 5). in cases of the simultaneous progression of fibrosis and airspace enlargement. which show predominantly groundglass opacity. Thin-section CT image at tracheal carina shows paraseptal emphysema with varied thickness of cyst wall. For instance. fibrosis can coexist in the area with emphysema [57] (Fig. Thin-section CT image at lung base shows honeycomb lung. it might be difficult to reject the term honeycomb lung. respectively [37. the interobserver agreement regarding the presence of honeycomb lung ranged from 0. There are cases that show paraseptal emphysema in the upper and middle lobes. Most anterior cysts appear similar to those of lung base. Other problems affect the CT diagnosis of honeycomb lung in cases with chronic interstitial pneumonia [52].

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