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Eur Radiol (2003) 13:515521

DOI 10.1007/s00330-002-1490-3 CHEST

Pia Reittner Pneumonia: high-resolution CT findings


Suzanne Ward
Laura Heyneman in 114 patients
Takeshi Johkoh
Nestor L. Mller

Received: 11 September 2001 Abstract The objective of the pres- fungal pneumonias. Extensive sym-
Revised: 21 March 2002 ent study was to assess the high-reso- metric bilateral areas of ground-glass
Accepted: 2 April 2001 lution CT appearances of different attenuation were present in 21 of 22
Published online: 3 August 2002 types of pneumonia. The high-resolu- (95%) patients with Pneumocystis
Springer-Verlag 2002
tion CT scans obtained in 114 pa- carinii pneumonia and were not seen
tients (58 immunocompetent, 59 im- in other pneumonias except in associ-
munocompromised) with bacterial, ation with areas of consolidation and
Mycoplasma pneumoniae, viral, fun- nodules. Centrilobular nodules were
P. Reittner () S. Ward L. Heyneman
N.L. Mller gal, and Pneumocystis carinii pneu- present less commonly in bacterial
Department of Radiology, monias were analyzed retrospectively pneumonia (6 of 35 patients, 17%)
Vancouver Hospital by two independent observers for than in Mycoplasma pneumoniae
and Health Sciences Center, presence, pattern, and distribution of (24 of 28, 96%), viral (7 of 9, 78%),
855 W. 12th Ave., Vancouver, BC, abnormalities. Areas of air-space or fungal (12 of 20, 92%) pneumonia
Canada V5Z 1M9
e-mail: pia-reittner@kfunigraz.ac.at consolidation were not detected in (p<0.01). Except for Pneumocystis
Tel.: +43-316-3852870 patients with viral pneumonia and carinii pneumonia and Mycoplasma
Fax: +43-316-3854149 were less frequently seen in patients pneumoniae pneumonia, which often
P. Reittner with Pneumocystis carinii pneumo- have a characteristic appearance,
Department of Radiology, nia (2 of 22 patients, 9%) than in high-resolution CT is of limited
Karl Franzens University bacterial (30 of 35, 85%), Mycoplas- value in the differential diagnosis of
and University Hospital Graz, ma pneumoniae (22 of 28, 79%), and the various types of infective pneu-
Auenbruggerplatz 9, 8036 Graz, Austria
fungal pneumonias (15 of 20, 75%; monia.
T. Johkoh p<0.01). There was no significant
Department of Radiology,
Osaka University Medical School, difference in the prevalence or distri- Keywords High-resolution CT
22 Yamadaoka, Suita, Osaka 5650825, bution of consolidation between bac- Pneumonias
Japan terial, Mycoplasma pneumoniae, and

Introduction graph provides adequate imaging information and CT is


not warranted [4]; however, an increasing number of pa-
It has been estimated that 4 million cases of pneumonia tients undergo CT, particularly high-resolution CT, when
occur each year in the United States [1, 2]. Despite the there is a high clinical suspicion for pneumonia in the
availability of antimicrobial agents, pneumonias consti- presence of normal or questionable radiographic findings
tute the sixth most common cause of death and are the [6, 7, 8, 9, 10, 11, 12]. The CT is also helpful in assess-
number one cause of death from infections [1, 2, 3, 4]. ing complications or evidence of mixed infections in pa-
Imaging plays a crucial role in the detection and man- tients with known pneumonia who are failing to respond
agement of patients with pneumonia [5]. The chest ra- to appropriate therapy [13, 14, 15].
diograph is usually the first imaging modality obtained Description of the high-resolution CT findings of
for the evaluation of acute respiratory symptoms. In the pneumonia have been limited to a small number of pa-
majority of patients with pneumonia, the chest radio- tients and almost exclusively to pneumonia in the immu-
516

Table 1 Causative agents of


pneumonias (n=114) Immunocompetent Immunocompromised
patient (n=58) patient (n=56)

Bacterial: n=35 (31)a


Streptococcus pneumoniae 14 (24)a
Staphylococcus aureus 16 (27)
Pseudomonas aeruginosa 3 (5)
Klebsiella pneumoniae 2 (3)
Mycoplasma pneumoniae: n=28 (24) 28 (48)
Pneumocystis carinii: n=22 (19) 22 (39)
Fungal: n=20 (17)
Aspergillus fumigatus 15 (27)
Candida albicans 5 (9)
Viral: n=9 (8)
a Numbers
Cytomegalovirus 7 (12)
in parentheses are Epstein-Barr virus 2 (3)
percentages

nocompromised host [6, 7, 8, 9, 16, 17, 18, 19]. The pur- The scans were interpreted independently by two radiologists
poses of this study were to assess the high-resolution CT for the presence, appearance, and distribution of parenchymal, me-
diastinal, and pleural abnormalities. The patterns of parenchymal
findings of pneumonias in a relatively large number of changes were subdivided into air-space consolidation, ground-
both immunocompromised and immunocompetent pa- glass attenuation, nodules, and reticulation. Ground-glass attenua-
tients, and to determine whether the pattern of abnormal- tion was defined as an area of hazy increased attenuation without
ities on high-resolution CT are helpful in suggesting a obscuration of underlying vascular markings. Airspace consoli-
dation was considered present when the underlying vessels were
specific infectious agent. obscured. Reticulation consisted of interlobular septal thickening
or intralobular reticular opacities.
The anatomic distribution for air-space consolidation and
Materials and methods ground-glass attenuation was noted to be non-segmental, segmen-
tal, or lobular. A non-segmental distribution was considered pres-
The study was retrospective and included 114 patients with vari- ent when areas of opacification were confluent and extended be-
ous types of pneumonia, who underwent high-resolution CT at yond segmental boundaries [1]. A segmental distribution was con-
two different academic centers. Patients were identified through a sidered present when the opacification was patchy, peribronchial,
review of patients, who had undergone chest CT for suspected or peribronchiolar, and did not cross segmental boundaries [1].
pulmonary infection. Patients with tuberculosis and non-tubercu- Lobular consolidation was considered present when the consolida-
lous mycobacterial infections were excluded from the study. The tion involved entire secondary lobules but spared adjacent lobules,
study population consisted of 66 men and 48 women, ranging in regardless of whether there was a segmental or non-segmental dis-
age from 8 to 87 years (mean age 45 years, SD 14 years). Fifty- tribution [1]. Nodules were considered either centrilobular or ran-
eight patients (51%) were immunocompetent and 56 (49%) immu- dom in distribution. Mediastinal compartments were evaluated for
nocompromised. Immunosuppression was the result of bone lymph node enlargement, and the pleural spaces for the presence
marrow transplantation (n=22), hematologic malignancies such as of pleural fluid.
leukemia or lymphoma (n=17), acquired immunodeficiency syn- Abnormalities were classified as being distributed predomi-
drome (n=8), solid organ transplantation (n=6), chemotherapy of nantly in the upper, middle, or lower lung zones, unilateral or
tumors (n=2), and immunosuppressive treatment for systemic bilateral.
lupus erythematosus (n=1). Agreement between the two observers for the predominant CT
The pneumonias were due to bacterial infection (n=35), Myco- findings was assessed using the kappa statistic [20]. The compari-
plasma pneumoniae (n=28), Pneumocystis carinii (n=22), fungi sons between the findings in the various types of pneumonia were
(n=20), and viruses (n=9). The organisms and their relative fre- made using the chi-square test [20]. Following initial independent
quencies are listed in Table 1. A microbiologic diagnosis was analysis by the two observers, a final decision regarding the find-
made in all patients. Specific diagnoses were obtained from posi- ings was reached by consensus. The patterns of abnormality de-
tive culture of sputum (n=35), bronchoalveolar lavage (n=21), scribed in the results section represent the conclusions reached by
open-lung biopsy (n=19), transbronchial biopsy (n=10), autopsy consensus.
(n=1), or in Mycoplasma pneumoniae pneumonia (n=28) from se-
rologic tests with elevated single titers or a fourfold rise in titer.
High-resolution CT scans were performed on a GE 9800, Hi
Speed Advantage (GE Medical Systems, Milwaukee, Wis.), or Results
CT-W 2000 (Hitachi Medical Corp, Tokyo, Japan) CT scanner.
The images were obtained at 10-mm intervals throughout the chest Areas of air-space consolidation (Fig. 1) were detected
using 1.0-mm (n=75) or 1.5-mm collimation (n=39). The scans in patients with bacterial (30 of 35 patients, 85%), Myco-
were reconstructed using a high spatial frequency algorithm. The plasma pneumoniae (22 of 28 patients, 79%), fungal (15
images were photographed at window settings appropriate for the
assessment of lung parenchyma (level: 600 to 700 HU; width: of 20 patients, 75%), and Pneumocystis carinii (2 of 22
10001500 HU) and mediastinum (level: 3040 HU; width: patients, 9%) pneumonias, but were not identified in pa-
400500 HU). tients with viral pneumonias (Table 2). The presence of
517

Table 2 Predominant high-resolution CT findings. PCP Pneumocystis carinii pneumonia

HRCT finding Bacterial Mycoplasma Viral Fungal PCP


pneumonia pneumoniae pneumonia pneumonia (n=22)
(n=35) pneumonia (n=28) (n=9) (n=20)

Air-space consolidation 30 (85)a 22 (79) 15 (75) 2 (9)


Non-segmental 24 (80) 15 (68) 6 (40) 2 (9)
Segmental 6 (20) 9 (40) 9 (60)
Lobular 11 (36) 13 (59) 3 (20)
Ground-glass attenuation 11 (31) 24 (86) 4 (44) 6 (30) 21 (95)
Non-segmental 11 (100) 13 (54) 4 (100) 6 (100) 21 (100)
Segmental
Lobular 11 (45)
Nodules 6 (17) 25 (89) 7 (78) 13 (65)
Centrilobular 6 (17) 24 (96) 7 (100) 12 (92)
Random 1 (4) 2 (15)
Reticulation 8 (22) 6 (21) 3 (33) 5 (25) 4 (18)
a Numbers in parentheses are percentages

Fig. 2 A 28-year-old man with AIDS and Pneumocystis carinii


pneumonia. High-resolution CT scan (1.5-mm collimation) reveals
extensive bilateral areas of ground-glass attenuation in a geo-
graphic distribution with sharp demarcation between normal and
abnormal lung

Mycoplasma pneumoniae, and fungal pneumonias (all


p>0.10, chi-square test; Table 2).
Fig. 1 A 49-year-old man with Streptococcus pneumoniae pneu-
Ground-glass attenuation (Fig. 2) was seen more
monia. High-resolution CT scan (1-mm collimation) targeted to commonly in Pneumocystis carinii pneumonia (21 of 22
the right lung reveals non-segmental air-space consolidation patients, 95%), than in fungal (6 of 20 patients, 30%)
involving the right lower lobe. Ground-glass attenuation is only and bacterial pneumonias (11of 35 patients, 31%;
detected around areas of air-space consolidation (arrows) p<0.01, chi-square test; Table 2). In patients with Pneu-
mocystis carinii pneumonia, the areas of ground-glass at-
tenuation were bilateral, symmetric, and extensive. The
air-space consolidation was significantly less common in other types of pneumonia were associated with more
Pneumocystis carinii pneumonia (2 of 22 patients, 9%), focal areas of ground-glass attenuation, usually adjacent
than in all other types of pneumonia (p<0.01, chi-square to areas of air-space consolidation. There was no signifi-
test). There was no significant difference in the preva- cant difference in the prevalence of ground-glass attenu-
lence or in the distribution (non-segmental, segmental, ation between bacterial, Mycoplasma pneumoniae, viral,
lobular) of air-space consolidation between bacterial, and fungal pneumonias (all p>0.10, chi-square test). In
518

Fig. 4 A 38-year-old man with Staphylococcus aureus pneumo-


nia. High-resolution CT scan (1-mm collimation) targeted to the
right lung shows patchy areas of air-space consolidation, consis-
tent with bronchopneumonia
Fig. 3 A 28-year-old woman with Mycoplasma pneumoniae pneu-
monia. High-resolution CT scan (1-mm collimation) targeted to
the right lung demonstrates poorly defined centrilobular nodules
(arrows), a focal area of air-space consolidation and lobular areas All patients with Pneumocystis carinii and viral pneu-
of ground-glass attenuation. Note sharp demarcation between nor- monia had bilateral diffuse lung involvement. Bilateral but
mal and abnormal secondary pulmonary lobules (curved arrows),
a finding characteristic for bronchopneumonia less extensive involvement was present in 12 of the pa-
tients (60%) with fungal, 9 (26%) with bacterial, and 6
(21%) with Mycoplasma pneumoniae pneumonia. Sixty-
four percent (18 of 28) of the patients with Mycoplasma
11 of 24 (45%) patients with Mycoplasma pneumoniae pneumoniae and 63% (22 of 35) with bacterial pneumo-
pneumonia the areas of ground-glass attenuation showed nias had a lower zone predominance of parenchymal ab-
a lobular distribution. This distribution of areas of normalities, whereas an upper zone predominance was
ground-glass attenuation was not seen in other forms of present in 10 of 20 (50%) patients with fungal pneumonia.
pneumonia. Cystic lesions within areas of coexistent ground-glass
Centrilobular nodules were detected more commonly attenuation were a unique finding seen in 5 of 22 (23%)
in Mycoplasma pneumoniae pneumonias (24 of 28 pa- patients with Pneumocystis carinii pneumonia. Pleural
tients, 86%; Fig. 3) than in bacterial pneumonias (6 of effusions were noted in 14 (40%) patients with bacterial,
35 patients, 17%; p<0.01, chi-square test; Fig. 4), and in 3 (15%) with fungal, and in 2 (7%) with Mycoplasma
were not seen in patients with Pneumocystis carinii pneumoniae pneumonia. Mediastinal lymph node en-
pneumonia (Table 2). There was no significant differ- largement was seen in 7 of 28 patients (25%) of Myco-
ence in the prevalence of nodules between Mycoplasma plasma pneumoniae and in 3 of 35 patients (8%) with
pneumoniae (25 of 28 patients, 89%), viral (7 of 9 pa- bacterial pneumonias.
tients, 78%; Fig. 5), and fungal pneumonias (13 of There was fair to moderate agreement between the
20 patients, 65%; Fig. 6; p>0.10, chi-square test). In bac- observers for the assessment of the presence of air-space
terial pneumonias 6 of 16 patients (37%) with staphylo- consolidation (kappa statistic, 0.47), ground-glass atten-
coccal infection demonstrated centrilobular nodules; uation (kappa statistic, 0.51), nodules (kappa statistic,
these were located adjacent to areas of patchy air-space 0.63), and reticulation (kappa statistic, 0.49). There was
consolidation. fair agreement in the assessment of the distribution of
There was no significant difference in the prevalence consolidation as being non-segmental (kappa statistic,
of reticulation between the various forms of pneumonia 0.42), segmental (kappa statistic, 0.44), or lobular (kappa
(p>0.10, chi-square test; Table 2). statistic, 0.41).
519

Fig. 6 A 36-year-old man with Aspergillus fumigatus broncho-


pneumonia after bone marrow transplantation. High-resolution CT
Fig. 5 A 31-year-old woman with cytomegalovirus pneumonia scan (1-mm collimation) through the right lung reveals areas of
after bone marrow transplantation. High-resolution CT scan air-space consolidation in a predominantly non-segmental distri-
(1.5-mm collimation) demonstrates numerous small nodules bution, centrilobular nodules (arrow), and areas of ground-glass
(arrows) attenuation (curved arrows)

Discussion On chest radiographs, due to the summation of opacities,


the distinction between the three forms of pneumonia is
Pneumonias have been traditionally classified into lobar difficult. Lobar pneumonias are frequently simulated by
pneumonias, bronchopneumonias, and interstitial pneu- confluent bronchopneumonias, and both can be mimicked
monias [1]. On chest radiographs lobar pneumonias, most by interstitial pneumonia when associated with patchy or
commonly caused by Streptococcus pneumoniae and diffuse areas of air-space opacification [21].
Klebsiella pneumoniae, are characterized by a non-seg- In a recently published study, analyzing the high-reso-
mental distribution and often involvement of a single lution CT findings in community-acquired pneumonias,
lobe. Bronchopneumonias have been traditionally consid- Tanaka et al. assessed the findings in 32 patients includ-
ered to be segmental in distribution [1]. In bronchopneu- ing 18 with bacterial pneumonia and 14 with atypical
monias the inflammatory process typically respects inter- pneumonia (Mycoplasma pneumoniae pneumonia, n=12;
lobular septal boundaries, involving some secondary pul- Chlamydia pneumonia, n=1; influenza virus pneumonia,
monary lobules while sparing adjacent lobules; therefore, n=1) [22]. The main feature differentiating the two
bronchopneumonia is also known as lobular pneumonia groups was the presence of centrilobular nodules seen in
[1, 21]. Common causes of bronchopneumonia include 9 of 14 patients (64%) with atypical pneumonias com-
Staphylococcus aureus, gram-negative organisms, Myco- pared with 2 of 18 patients (11%) with bacterial pneumo-
plasma pneumoniae, and fungi. Interstitial pneumonias nias. In the current study, similar to the results of Tanaka
are associated with a reticulonodular pattern, and are et al., nodules were detected in only 6 of 35 patients
most commonly caused by viruses [1]. In interstitial (17%) with bacterial pneumonia, but were commonly
pneumonias progression of the inflammatory process may seen in patients with Mycoplasma pneumoniae (89%),
result in patchy or diffuse areas of air-space opacification. viral (77%), and fungal (65%) pneumonia.
520

A predominantly nodular pattern of pneumonia may ground-glass attenuation usually seen in association with
be seen with various infections. Fungal pneumonia char- centrilobular nodules may be present. These focal areas
acteristically manifests as multiple, ill-defined nodules of ground-glass attenuation often have a lobular distribu-
that may gradually coalesce to form a mass or an area of tion [13, 22]. In bacterial and fungal pneumonias areas
air-space consolidation [19, 23]. In viral pneumonia, of ground-glass attenuation tend to be minor findings ad-
nodules are typically associated with a background of jacent to areas of air-space consolidation and nodules
diffuse ground-glass attenuation and/or reticulation [17, [22, 23].
18]. In Mycoplasma pneumoniae and bacterial pneumo- Reticulation was a non-specific feature in all groups
nias caused by Nocardia, Staphylococcus aureus, and of pneumonias, and was associated with air-space con-
Pseudomonas aeruginosa, nodules may extend to in- solidation, ground-glass attenuation, and nodules.
volve the entire secondary pulmonary lobule [8, 13]. Our study has several limitations. It is retrospective
The significance of ground-glass attenuation depends and includes a limited number of patients in each group
on the immune status of the patient. In immunocompro- of pneumonia, especially viral pneumonia. Only a small
mised patients, the presence of extensive, diffuse, bilat- number of patients with pneumonia undergo CT; there-
eral ground-glass attenuation is highly suggestive for fore, it is possible that the study was biased toward pa-
Pneumocystis carinii pneumonia [6, 25, 26]. In a study tients with more extensive abnormalities or atypical pre-
by Hartman et al. the presence of this pattern allowed a sentations. Furthermore, the study did not compare the
confident diagnosis of Pneumocystis carinii pneumonia findings of CT with those seen on the radiograph.
in 22 of 24 patients (94%) with AIDS [9]. Unusual ra-
diologic patterns in Pneumocystis carinii pneumonia
suggesting the presence of an alternative infectious agent Conclusion
include focal or diffuse areas of air-space consolidation
and occasionally nodules [26, 27, 28]. In immunocom- In conclusion, there is considerable overlap between the
promised patients who do not have AIDS and in immu- high-resolution CT features of the various types of pneu-
nocompetent patients with pneumonia, areas of ground- monia. The presence of extensive areas of ground-glass
glass attenuation are a common but non-specific finding. attenuation with absence of air-space consolidation is
Although viral pneumonia may produce extensive areas highly suggestive of Pneumocystis carinii pneumonia
of ground-glass attenuation, viral infections are com- and the combination of centrilobular nodules and lobular
monly associated with nodules and focal or diffuse areas areas of ground-glass attenuation is most suggestive of
of air-space consolidation [17, 18, 28]. In the current Mycoplasma pneumoniae pneumonia. In the current
study only 4 patients with viral pneumonia had ground- study, the other causes of pneumonia could not be distin-
glass attenuation, but 7 had centrilobular nodules. In guished on the basis of pattern or distribution of abnor-
Mycoplasma pneumoniae pneumonia, focal areas of malities on high-resolution CT.

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