Eur Radiol (2009) 19: 809815 DOI 10.

1007/s00330-008-1233-1

CHEST

Fumito Okada Yumiko Ando Koichi Honda Tomoko Nakayama Maki Kiyonaga Asami Ono Shuichi Tanoue Toru Maeda Hiromu Mori

Clinical and pulmonary thin-section CT findings in acute Klebsiella Pneumoniae pneumonia

Received: 13 July 2008 Accepted: 25 October 2008 Published online: 26 November 2008 # European Society of Radiology 2008

F. Okada (*) Department of Radiology, Oita University Faculty of Medicine, 11 Idaigaoka, Hasama-machi, Yufu-shi, Oita, 8795593, Japan e-mail: fumitook@med.oita-u.ac.jp Tel.: +81-97-5865934 Fax: +81-97-5860025

All authors have no direct or indirect financial interest in the products under investigation or subject matter discussed in this manuscript. F. Okada . Y. Ando . K. Honda . T. Nakayama . M. Kiyonaga . A. Ono . S. Tanoue . T. Maeda . H. Mori Department of Diagnostic and Interventional Radiology, Oita University Faculty of Medicine, Oita, Japan

Abstract The aim of this study was to assess the clinical and pulmonary thinsection CT findings in patients with acute Klebsiella pneumoniae pneumonia. We retrospectively evaluated thin-section CT examinations performed between January 1991 and December 2007 from 962 patients with acute Klebsiella pneumoniae pneumonia. Seven hundred and sixtyfour cases with concurrent infectious diseases were excluded. Thus, our study group comprised 198 patients

(118 male, 80 female; age range 18 97 years, mean age 61.5). Underlying diseases and clinical findings were assessed. Parenchymal abnormalities were evaluated along with the presence of enlarged lymph nodes and pleural effusion. CT findings in patients with acute Klebsiella pneumoniae pneumonia consisted mainly of ground-glass attenuation (100%), consolidation (91.4%), and intralobular reticular opacity (85.9%), which were found in the periphery (96%) of both sides of the lungs (72.2%) and were often associated with pleural effusion (53%). The underlying conditions in patients with Klebsiella pneumoniae pneumonia were alcoholism or smoking habit. Keywords Klebsiella pneumoniae . Pneumonia . CT

Klebsiella pneumoniae is a well-known cause of community-acquired bacterial pneumonia, which accounts for only 0.55.0% of all pneumonia. It is an important type of pneumonia because of its severity, high incidence of complications, and elevated mortality [1, 2]. The clinical presentation is classically characterized by rapid onset of acute pulmonary symptoms with the production of thick currant-jelly sputum in alcoholic men who are frequently also chronic smokers. The mortality rate in alcoholics with Klebsiella pneumoniae pneumonia has been reported as

5060% [3, 4]. Recently, Jong et al. have also reported that alcoholics with Klebsiella pneumoniae pneumonia have a rapidly fatal clinical course with a mortality of 100%, even with adequate antibiotic therapy and intensive management [5]. Therefore, it is crucial to identify the risk factors associated with poor outcome and to evaluate the radiological findings as soon as possible, so as to lose no time in initiating appropriate management [6, 7]. The characteristics of Klebsiella pneumonia on plain radiography have been described previously [1, 5, 811]. Felson et al. [10] studied 14 patients with acute

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Klebsiella pneumonia and have suggested that the presence of certain radiological features indicates a diagnosis of acute Klebsiella pneumonia. These features are bulging fissures, sharp margins of the advancing border of the pneumonic infiltrate, and early abscess formation. In patients with acute Klebsiella pneumoniae pneumonia, only Tsukahira et al. have shown pulmonary CT findings in three acute and one chronic case of Klebsiella pneumonia [12]. However, to the best of our knowledge, no Englishlanguage studies of pulmonary CT findings in patients with acute Klebsiella pneumoniae pneumonia have been published. This study aimed to assess clinical findings and pulmonary thin-section CT findings in acute Klebsiella pneumoniae pneumonia.

The patients included 36 with postoperative malignancy. In addition, patients with cardiac disease (n=39), pulmonary emphysema (n=35), diabetes mellitus (n=28), collagen disease (n=13), and pneumoconiosis (n=7) were included in the study (Table 1). An alcoholic was defined as an individual with a daily consumption of 80 g alcohol during the past 2 years [13], and a patient was considered to be a heavy smoker if he/she had smoked more than 10 pack-years. Forty-eight patients were alcoholics, 39 were chronic smokers, and 33 were both alcoholics and chronic smokers.

CT
Examinations

Materials and methods

Patients Our institutional review board approved this retrospective study and waived informed consent. We retrospectively identified 962 patients with acute Klebsiella pneumoniae pneumonia who had undergone chest thin-section CT examinations between January 1991 and December 2007 at five institutions. We excluded patients with concurrent infections diagnosed by serological tests and clinical findings. Thus, we excluded 353 patients with methicillin-resistant Staphylococcus aureus (MRSA), 224 with Pseudomonas aeruginosa, 208 with Candida albicans, 128 with Enterobacter cloacae, 111 with Stenotrophomonas maltophilia, 71 with Serratia marcescens, and some with other additional pathogens. Moreover, six cases with acute Klebsiella pneumoniae pneumonia were excluded because of poor image quality caused by motion artifacts, inadequate window level settings, or for which hard copies of the CT film had been destroyed. Thus, the study group comprised 198 patients (118 male, 80 female; age range 1897 years, mean age 61.5) with acute Klebsiella pneumoniae pneumonia. No patients with smoking-related diseases, such as desquamative interstitial pneumonia or Langerhans cell histiocytosis, were included in this study. The diagnosis was established by isolation of Klebsiella pneumoniae from sputum in 182 patients, bronchoalveolar lavage fluid (BALF) in 10, and blood specimens in 6. A patient was considered to have community-acquired pneumonia if at the time of hospital admission he/she presented with cough, with or without sputum, fever, leukocytosis or leukopenia, and had pulmonary infiltrates on chest radiographs. No patient had been admitted to or treated in a hospital 2 weeks before admission. Among the 198 patients, 52 had community-acquired and 146 had nosocomial infections.

Thin-section CT examinations were performed with 1-mm collimation at 10-mm intervals from the apex of the lung to the diaphragm (n=150) or volumetrically with a multidetector CT system with 1-mm reconstruction (n=48). The CT examinations were performed with the patient in the supine position at full inspiration and were reconstructed by using a high-spatial-frequency algorithm. Images were captured at window settings that allowed viewing of the lung parenchyma (window level, 600 to 700 HU; window width, 1,2001,500 HU) and the mediastinum (window level, 2040 HU; window width, 400 HU). The pulmonary CT examination was performed within 16 days
Table 1 Patient characteristics and underlying conditions Sex, M/F Alcoholic Smoking habit Cardiac disease Pulmonary emphysema Diabetes mellitus Collagen disease Pneumoconiosis Malignancy Presenting symptoms Fever Cough Sputum Currant-jelly sputum Chest pain Dyspnea General weakness Delirium Data in parentheses are percentages 118/80 81 (40.9) 72 (36.4) 39 (19.7) 35 (17.7) 28 (14.1) 13 (6.6) 7 (3.5) 36 (18.2) 198 (100) 198 (100) 158 (79.8) 67 (33.8) 30 (15.2) 25 (12.6) 16 (8.1) 13 (6.6)

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(mean 3.75 days) after the onset of respiratory symptoms. Intravenously administered contrast material was used for 43 examinations. Image interpretation

symptoms. The most common presenting symptoms were fever and cough (198 patients each, 100%), followed by sputum (158 patients, 79.8%). Currant-jelly sputum was observed in 67 patients (33.8%). CT patterns

Two chest radiologists (with 20 and 12 years of experience in chest CT image interpretation, respectively), who were aware of the underlying diagnoses, retrospectively and independently interpreted the CT images. Conclusions were reached by consensus. An average of two sessions per week was reserved for review of the CT findings, with a total of about 80 sessions. CT images were assessed for the following radiological patterns: ground-glass attenuation, consolidation, nodule, centrilobular nodules, bronchial wall thickening, interlobular septal thickening, intralobular reticular opacity, bronchiectasis, enlarged hilar/mediastinal lymph node(s) (>1 cm diametre short axis), and pleural effusion. Areas of groundglass attenuation were defined as hazy increases in attenuation without obscuration of vascular markings [14, 15]. Areas of consolidation were defined as areas of increased attenuation that caused obscuration of normal lung markings [14, 15]. Centrilobular nodules were defined as those present around the peripheral pulmonary arterial branches or 35 mm from the pleura, interlobular septa, or pulmonary veins. Interlobular septal thickening was defined as abnormal widening of interlobular septa [15]. Intralobular reticular opacity was considered present when interlacing line shadows were separated by a few millimetres [14, 15]. The distribution of parenchymal disease was also noted. Whether the abnormal findings were located unilaterally or bilaterally was assessed. If the main lesion was predominantly located in the inner third of the lung, the disease was classified as having a central distribution. On the other hand, if the lesion was predominantly located in the outer third of the lung, the disease was classified as having a peripheral distribution. If the lesions showed no predominant distribution, the disease was classified as having a random distribution. In addition, zonal predominance was classified as upper, lower, or random. Upper lung zone predominance meant that most abnormalities were seen at a level above the tracheal carina, while lower zone predominance referred to most abnormalities being below the upper zone. When abnormalities showed no definite zonal predominance, the lung disease was classified as having a random distribution.

Chest CT revealed abnormalities in all patients with acute Klebsiella pneumoniae pneumonia (Table 2). Among the 198 patients, ground-glass attenuation (n=198, 100%) (Figs. 1, 2, 3, 4 and 5) was the most frequently seen, followed by consolidation (n=181, 91.4%) (Figs. 1, 2, 3, 4 and 5), intralobular reticular opacity (n=170, 85.9%) (Figs. 1, 2, 3, 4 and 5), and bronchial wall thickening (n=52, 26.3%) (Figs. 1 and 5). Interlobular septal thickening (n=19, 9.6%) (Figs. 1 and 4), centrilobular nodules (n=8, 4.0%), and bronchiectasis (n=8, 4.0%) were also observed. Cavitary lesions or nodules were found in only one patient (0.5%). The combination of consolidation and ground-glass attenuation (n=178, 89.9%) was seen most frequently, followed by consolidation and intralobular reticular opacity (n=161, 81.3%). Some ground-glass attenuation was also detected in areas near bronchial wall thickening. Disease distribution Among the 198 patients with acute Klebsiella pneumoniae pneumonia, abnormal findings were found bilaterally in 143 patients (72.2%) and unilaterally in 55 patients (27.8%), and in the periphery (n=190, 96.0%). On the other hand, there were eight patients with disease that showed a random distribution (4.0%), and no patients with a predominantly central distribution. The predominant zonal distribution was at the upper zone in 26 patients (13.1%) (Figs. 1 and 4), lower zone in 110 patients (55.6%) (Figs. 2, 3 and 5), and random distribution was observed in 62 patients (31.3%). Effusion and lymph Nodes Bilateral pleural effusions were found in 26 patients (13.1%), and unilateral pleural effusion was found in 79 patients (39.9%) (Figs. 3 and 4) with acute Klebsiella pneumoniae pneumonia. Mediastinal and/or hilar lymph node enlargement was observed in eight patients (4.0%). Enlarged lymph nodes were found at the paratracheal, tracheobronchial, and subcarinal regions. Follow-up study All 198 patients underwent antibiotic therapy. In 48 of 52 patients with community-acquired infections (92.3%), the

Results
Clinical features The clinical characteristics and underlying conditions are summarized in Table 1. All patients had respiratory

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Table 2 Thoracic CT findings in 198 patients Findings Ground-glass attenuation Consolidation Intralobular reticular opacity Bronchial wall thickening Interlobular septal thickening Centrilobular nodules Bronchiectasis Nodules Cavity Pleural effusion Lymph node enlargement Data in parentheses are percentages No. of patients 198 (100) 181 (91.4) 170 (85.9) 52 (26.3) 19 (9.6) 8 (4.0) 8 (4.0) 4 (2.0) 1 (0.5) 105 (53.0) 8 (4.0)

abnormal findings improved on follow-up CT examinations or chest radiographs. However, in the remaining four patients (7.7%), who were alcoholics and smokers, abnormal findings on follow-up CT, such as ground-glass attenuation, consolidation, and intralobular reticular opacity, worsened, and the patients died. By comparison, in 120 of 146 patients with nosocomial infections (82.2%), the abnormal findings improved on follow-up CT or radiographs. In the remaining 26 patients (17.8%), which consisted of 18 alcoholics and 16 smokers, parenchymal abnormal findings and pleural effusions worsened, and the patients died.

tion. This may have biased the results. The mortality rates of both groups in our study were lower than those in previous studies [2, 18]. Klebsiella pneumonia tends to affect people with underlying diseases, such as alcoholism, diabetes and chronic lung disease [1820]. Jong et al. have shown that a high incidence (39.3%) of Klebsiella pneumoniae pneumonia was noted in alcoholics with community-acquired pneumonia, and all these patients had a rapidly fatal outcome, despite aggressive intensive care and adequate antibiotic therapy [5]. In the present study, alcoholism (40.9%) was the most commonly associated condition, followed by a smoking habit (36.4%), cardiac disease (19.7%), and malignant disease (18.2%). In addition, four patients with community-acquired pneumonia, who were alcoholics and smokers, had a fatal clinical course. Infected persons generally have high fever, chills, flulike symptoms, and a cough that produces a lot of sputum. The latter is often thick and blood-tinged, and has been referred to as currant-jelly sputum because of its appearance, which is known as a specific symptom in Klebsiella pneumonia. In the present study, all patients had several complaints, such as fever, cough, and sputum. Currant-jelly sputum was observed in 67 patients (33.8%), which has not been reported before.

Discussion
Klebsiella pneumoniae, one of the most important gramnegative bacterial pathogens, is of worldwide concern, because of (1) its ability to produce extended-spectrum lactamases, (2) its tendency to develop antibiotic resistance, and (3) its association with high mortality rates [16]. Early initiation of adequate antibiotic therapy has been shown to improve patient progress [17]. Therefore, it is crucial to identify the risk factors associated with worse outcome and radiological features in patients with acute Klebsiella pneumoniae infections as early as possible, so as to lose no time in initiating appropriate management [6]. Kang and colleagues have reported the clinical features and treatment and clinical outcomes in patients with Klebsiella pneumoniae bacteremia [18]. They found that mortality rates for nosocomial infection were more than twice those for community-acquired infection (32% vs. 16%). The group with nosocomial infection was sicker, had greater prior antibiotic exposure, showed more frequent antibiotic resistance, and underwent more invasive procedures compared with the group with community-acquired infec-

Fig. 1 Acute Klebsiella pneumoniae pneumonia in a 78-year-old female alcoholic with a smoking habit, at 2 days after onset of fever and cough with currant-jelly sputum. Transverse thin-section CT 1 cm above the tracheal carina showing consolidation (white arrow), ground-glass attenuation, and intralobular reticular opacity. Interlobular septal thickening (arrowhead) and bronchial wall thickening (arrow) were also present

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Fig. 2 Acute Klebsiella pneumoniae pneumonia in a 50-year-old male alcoholic, at 2 days after onset of fever, cough, and chest pain. Transverse thin-section CT of right lower lobe showing groundglass attenuation and consolidation with intralobular reticular opacity (arrow)

As for CT features, Moon et al. have evaluated complicated Klebsiella pneumonia in 11 patients [26]. They have reported that the most common CT manifestation of complicated Klebsiella pneumonia was necrotizing pneumonia associated with pleural abnormalities, and in extensive cases, pulmonary gangrene or lung abscess was a rare complication. Recently, Tsukadaira et al. have evaluated CT findings in three patients with acute and one with chronic Klebsiella pneumoniae pneumonia [12]. Of the three acute cases, CT showed a dense, confluent infiltrate that involved almost the entire right lower lobe in one case, and CT of the remaining two cases showed acute bronchopneumonia with peribronchial ground-glass attenuation and consolidation in the right or left upper lobe. However, to the best of our knowledge, no Englishlanguage radiological studies of pulmonary CT findings in patients with acute Klebsiella pneumoniae pneumonia have been published. We retrospectively evaluated CT findings in 198 patients with acute Klebsiella pneumoniae pneumonia. The most common CT findings were ground-glass attenuation, followed by consolidation and intralobular reticular opacity. The abnormal findings were predominantly seen in the periphery of both sides of the lungs,

Klebsiella pulmonary infections have been classified by radiographic and clinical criteria [2123]. In 1990, Carpenter divided Klebsiella pulmonary infections into acute pneumonia and complications of acute pneumonia [24]. The complications consisted of lung abscess, pulmonary gangrene, and chronic Klebsiella pulmonary infections. The frequencies of abscess formation, gangrene, and development of chronic pneumonia were 1650, 750, and 533%, respectively [24]. Acute pneumonia due to Klebsiella was first described by Friedlander in 1882 when he found the organism at necropsy in several patients [25]. Felson et al. [10] have studied 14 patients with acute Klebsiella pneumonia, who were diagnosed on the basis of sputum, blood, pleural fluid, or lung aspiration of the organism. They have suggested that the roentgen features of bulging fissures, sharp margins of the advancing border of the pneumonic infiltrate, and early abscess formation indicate a diagnosis of acute Klebsiella pneumonia. With the antibiotic era and a large immunosuppressed population, Korvick et al. have suggested a change in the appearance of Klebsiella pneumonia upon plain radiography [2]. The majority of their cases were of the nosocomial variety; they were more often bilateral and were not associated with bulging fissures or cavitation.

Fig. 3 Acute Klebsiella pneumoniae pneumonia in a 59-year-old female alcoholic with collagen disease (systemic lupus erythematosus), at 3 days after onset of fever, cough with currant-jelly sputum, and dyspnea. Transverse thin-section CT of right lower lobe showing consolidation (arrowhead) and intralobular reticular opacity (arrows) with peripheral distribution. Pleural effusion was also present

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Fig. 4 Acute Klebsiella pneumoniae pneumonia in a 79-year-old female alcoholic with postoperative ovarian cancer, at 3 days after onset of fever, cough, sputum, and general weakness. Transverse thin-section CT of right upper lobe showing consolidation, intralobular reticular opacity (arrow), and interlobular septal thickening (arrowhead), with peripheral distribution. Pleural effusion was also present

reported that CT findings in 41 patients with Streptococcus pneumoniae pneumonia consisted mainly of consolidation, reticular opacity, and centrilobular nodules (90, 39, and 32%, respectively). The frequency of the centrilobular nodules in Streptococcus pneumoniae pneumonia was higher than that in acute Klebsiella pneumoniae pneumonia (32 vs. 4%). Moreover, the frequencies of reticular opacity and pleural effusion were lower than those in Klebsiella pneumoniae pneumonia (39 vs. 85.9%, and 20 vs. 53%, respectively). Previously, we have reported chest CT findings in 42 patients with Mycoplasma pneumoniae pneumonia [29]. The CT findings in Mycoplasma pneumoniae pneumonia consisted mainly of centrilobular nodules and bronchial wall thickening, the frequencies of which were higher than those in Klebsiella pneumoniae pneumonia (90.5 vs. 4%, and 88.1 vs. 26.3%, respectively). It should be noted that there were several limitations to our study. First, this was a retrospective study, and CT image interpretation was performed by consensus. Second, our study lacked a pathological correlation with specific CT findings, such as consolidation and intralobular reticular opacity. Third, the thin-section CT images were obtained at several institutions using different protocols. In summary, we investigated clinical and thin-section CT findings in 198 patients with acute Klebsiella

which are similar to those in previous chest radiographs [5]. In addition, bilateral pleural effusion was seen in 26 patients (13.1%) and unilateral effusion in 79 (39.9%). The frequency of pleural effusions was similar to that in a previous study [5]. In the present study, cavitary lesions were found in only one patient (0.5%), whose CT examination was performed at 3 days after onset of respiratory symptoms. Acute lung abscesses have been reported to develop within 4 days of the presentation of acute pneumonia [27]. The frequency of development of acute abscesses varies from 16% to >50% [24, 26]; however, this might be because most of the literature was published in the pre-antibiotic era or a period of minimal antibiotic use. In addition, there have been no studies in which additional pathogens were not evaluated in patients with Klebsiella pneumoniae pneumonia or bacteremia. In the present study, in 764 of 962 patients (79.4%) with acute Klebsiella pneumoniae pneumonia who were excluded from the study, one or more additional pathogens, such as MRSA and Pseudomonas aeruginosa, were found. Therefore, the frequency of cavitary lesions and the mortality rates in our patients might be lower than that in previous studies [2, 18, 24, 26]. Streptococcus pneumoniae and Mycoplasma pneumoniae are also known as common pathogens of communityacquired or nosocomial pneumonia. Nambu et al. [28] have

Fig. 5 Acute Klebsiella pneumoniae pneumonia in a 63-year-old male alcoholic with a smoking habit, at 3 days after onset of fever, cough, and sputum. Transverse thin-section CT of left lower lobe showing consolidation, intralobular reticular opacity, and bronchial wall thickening (arrowheads)

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pneumoniae pneumonia. The underlying conditions in these patients were alcoholism, smoking habit, or malignant diseases, and the CT findings consisted mainly of

consolidation with ground-glass attenuation or intralobular reticular opacity in the periphery of both sides of the lungs, with pleural effusion.

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