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Cardiopulmonar y Imaging • Original Research

Little et al.
Radiographic Follow-Up of Pneumonia

Cardiopulmonary Imaging
Original Research

Outcome of Recommendations
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for Radiographic Follow-Up of


Pneumonia on Outpatient Chest
Radiography
Brent P. Little1 OBJECTIVE. Follow-up chest radiographs are frequently recommended by radiologists
Matthew D. Gilman2 to document the clearing of radiographically suspected pneumonia. However, the clinical
Kathryn L. Humphrey 2 utility of follow-up radiography is not well understood. The purpose of this study was to ex-
Tarik K. Alkasab2 amine the incidence of important pulmonary pathology revealed during follow-up imaging of
Fiona K. Gibbons 3 suspected pneumonia on outpatient chest radiography.
MATERIALS AND METHODS. Reports of 29,138 outpatient chest radiography exam-
Jo-Anne O. Shepard2
inations performed at an academic medical center in 2008 were searched to identify cases in
Carol C. Wu2 which the radiologist recommended follow-up chest radiography for presumed community-ac-
Little BP, Gilman MD, Humphrey KL, et al. quired pneumonia (n = 618). Descriptions of index radiographic abnormalities were recorded.
Reports of follow-up imaging (radiography and CT) performed during the period from Janu-
ary 2008 to January 2010 were reviewed to assess the outcome of the index abnormality. Clini-
cal history, demographics, microbiology, and pathology reports were reviewed and recorded.
RESULTS. Compliance with follow-up imaging recommendations was 76.7%. In nine of
618 cases (1.5%), a newly diagnosed malignancy corresponded to the abnormality on chest
radiography initially suspected to be pneumonia. In 23 of 618 cases (3.7%), an alternative
nonmalignant disease corresponded with the abnormality on chest radiography initially sus-
pected to be pneumonia. Therefore, in 32 of 618 patients (5.2%), significant new pulmonary
diagnoses were established during follow-up imaging of suspected pneumonia.
CONCLUSION. Follow-up imaging of radiographically suspected pneumonia leads to a
small number of new diagnoses of malignancy and important nonmalignant diseases, which
may alter patient management.

Keywords: chest radiography, community-acquired

M
alignancy and other important Thoracic Society consensus guidelines for
pneumonia, lung cancer
nonmalignant pulmonary diseas- managing community-acquired pneumonia in
DOI:10.2214/AJR.13.10888 es may present with a radiograph- adults contain no mention of follow-up chest
ic appearance similar to pneumo- radiography [3, 4].
Received March 8, 2013; accepted after revision nia. For this reason, follow-up chest radiography Clinical practice regarding follow-up rec-
June 16, 2013.
is often recommended in patients to confirm ommendations of a new pulmonary opaci-
1
Department of Radiology and Imaging Sciences, Emory resolution of a radiographically suspected ty suspected to be pneumonia varies among
University, Atlanta, GA. pneumonia and to exclude an alternative dis- radiologists. A survey of the members of
2
ease (such as cancer), that would not clear after the Society of Thoracic Radiology showed
Department of Radiology, Massachusetts General
treatment of pneumonia. However, there is no that 42% of respondents always recommend
Hospital, Harvard Medical School, 55 Fruit St., Boston,
MA 02114. Address correspondence to C. C. Wu consensus regarding the clinical utility of fol- follow-up radiography for new pulmonary
(carolcwu@gmail.com). low-up radiography. The 2005 guidelines of the opacities suspected to represent community-
American College of Chest Physicians recom- acquired pneumonia. The majority of respon-
3
Department of Pulmonary and Critical Care Unit, mend follow-up radiography approximately 8 dents (55%) recommend follow-up radiogra-
Massachusetts General Hospital, Harvard Medical
School. Boston, MA.
weeks after diagnosis to ensure clearing [1]. phy “sometimes” on the basis of appearance
The British Thoracic Society (2009) recom- of the opacity, patient age, and clinical symp-
This article is available for credit. mends follow-up chest radiography at 6 weeks toms [5]. The yield of such follow-up imaging
for all patients who have persistent clinical recommendations and the rates of compliance
AJR 2014; 202:54–59
symptoms or who are at increased risk for ma- are incompletely understood.
0361–803X/14/2021–54 lignancy, such as smokers and patients older The purpose of this study was to retro-
than 50 years [2]. However, the 2007 Infectious spectively evaluate the outcome of recom-
© American Roentgen Ray Society Disease Society of America and the American mendations for follow-up radiography at our

54 AJR:202, January 2014


Radiographic Follow-Up of Pneumonia

TABLE 1:  Characteristics of Patient Populations


All Patients With Recommendations for Patients With Follow-Up Patients With No p
Characteristic Follow-Up Radiography (n = 805) Imaging (n = 618) Follow-Up Imaging (n = 187) (Follow-Up vs No Follow-Up)
Mean age (median) (y) 61 (62) 63 (64) 54 (55) < 0.0001
Sex (M:F) 381:424 285:333 96:91 0.21
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History of cancer 201 (25) 169 (27) 32 (17) 0.005


Current smoker 125 (16) 99 (16) 26 (14) 0.73
Documented COPD 127 (16) 114 (18) 13 (7) < 0.0001
Diabetes 108 (13) 89 (14) 19 (10) 0.14
Undergoing chemotherapy 25 (3) 23 (3.7) 2 (1) 0.089
Known HIV 14 (2) 12 (1.9) 2 (1) 0.54
Preoperative examination 36 (4) 22 (4) 14 (7) 0.041
Note—Except where indicated otherwise, data in parentheses are percentages. Bold text indicates significant difference. COPD = chronic obstructive pulmonary disease.

institution, where the current practice is to Healthcare Clinical Applications Suite, Clini- Radiographic and CT Data Collection
routinely recommend follow-up chest radi- cal Systems Research and Development, Part- The dates of all radiography and chest CT exam-
ography in all adults, regardless of age or ners Healthcare System; and Partners Healthcare inations were recorded. Reports of all chest radi-
smoking history, to confirm clearance of Longitudinal Medical Record, Clinical Informat- ography and all chest CT examinations performed
pulmonary opacities suspected to represent ics Research and Development, Partners Health- during the follow-up period (January 2008–Janu-
community-acquired pneumonia. care System). Data were recorded using Microsoft ary 2010) were reviewed, terminating with a study
Office Excel 2003. The patient demographics are showing the resolution, pathologic diagnosis, or last
Materials and Methods listed in Table 1. Results of cytology, surgical pa- available study performed on the patient within the
This retrospective HIPAA-compliant study was thology, bronchoscopy washings, and microbiol- hospital system. “Resolution” was defined as ab-
approved by the institutional review board. The ogy were obtained and recorded from the Partners sence of a corresponding abnormality on follow-up
requirement for informed consent was waived. EMR. Final diagnoses were obtained from cy- radiography or CT. Cases in which no abnormality
tology, surgical pathology, bronchoscopy results, was found on CT or in which the abnormality near-
Patient Selection microbiology, and patient notes indicating a final ly resolved with only minimal atelectasis or scar-
Electronic records of 29,138 chest radiogra- clinical diagnosis. ring were also included in this category.
phy examinations performed in the outpatient set- Initial follow-up radiographs were classified as
ting at an academic medical center during 1 year Radiographic and CT Interpretation showing either resolution of abnormality, improve-
(2008) were queried for cases in which the inter- Radiography and chest CT examinations in the ment but incomplete resolution, no significant in-
preting radiologist recommended follow-up chest study group were interpreted by 11 thoracic radi- terval change, or worsening. Specific descriptions
radiography to ensure resolution of radiographi- ologists with 2–40 years of experience. Digital of the original and follow-up chest radiography ab-
cally suspected pneumonia. Using custom soft- posteroanterior and lateral chest radiography were normalities were recorded and are listed in Table
ware written using the Ruby programming lan- performed on computed radiography and digital ra- 2. CT results were recorded, including the impres-
guage (www.ruby-lang.org, accessed November diography units. Chest CT examinations were per- sion of the thoracic radiologist interpreting the ex-
12, 2012), our department’s radiology information formed on 16-MDCT and 64-MDCT scanners. All amination (infection or aspiration, malignancy,
system (Centricity, GE Healthcare) was searched studies were reviewed on a dedicated PACS work- subsegmental atelectasis or scarring, edema, and
for examinations with chest radiography exami- station (Impax, version 5.3.2, AGFA Healthcare). so on). Index radiography reports were compared
nation codes in which the reports contained the
text “recommend” but not the phrase “no imaging
recommendations.” The subjects were outpatients TABLE 2:  Description of Abnormality on Index Radiography Cases in Which
referred from general medicine clinics, specialty Follow-Up Radiography or CT Was Performed (n = 618)
clinics, and the emergency department associated
Abnormality No. (%)
with a tertiary care academic center. Index radi-
ography examinations with findings that the inter- Opacity not otherwise specified 338 (54.7)
preting radiologist thought were highly suspicious Pneumonia/consolidation 109 (17.6)
for cancer or recommended immediate chest CT
Atelectasis vs pneumonia 87 (14.1)
(n = 1317) or PET/CT (n = 1) were excluded from
the study. Reticular opacity/interstitial abnormality 53 (8.6)
Nodular opacity or nodules 29 (4.7)
Patient Data Collection Pleural effusion 11 (1.8)
Patient results and clinical notes from January
Rounded opacity 9 (1.5)
2008 to January 2010 were reviewed in the elec-
tronic medical record (Partners EMR, Partners Masslike opacity 2 (0.3)

AJR:202, January 2014 55


Little et al.

with CT reports to assess anatomic correspondence no follow-up chest imaging (CT or radiogra- phy; three had known COPD, and two were
between radiographic and CT abnormalities. phy) at our institution. The average age of pa- current smokers. The presenting symptoms
tients without follow-up imaging (mean, 54 of these nine patients were cough (n = 6),
Cases of Malignancy, Infection, and Other years; median, 55 years) was lower than that chest pain (n = 2), wheezing (n = 2), dyspnea
Nonmalignant Disease of the patients with follow-up imaging (mean, (n = 2), fatigue (n = 2), fever (n = 1), night
In cases in which malignancy, infection, or oth- 63 years; median, 64 years p < 0.0001). Pa- sweats (n = 1), and weight loss (n = 1).
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er nonmalignant disease was the eventual diagnosis, tients with documented follow-up imaging In the six cases of malignancy not corre-
the original chest radiographs and chest CT images (27%) were more likely to have a history of lating with the location on the index chest ra-
were reviewed independently by two thoracic radi- known malignancy than those without follow- diographic abnormality, only one case was an
ologists to confirm that the malignancy, infection, or up imaging (17% p = 0.005) and were more extrathoracic malignancy (pancreatic neuro-
other nonmalignant disease corresponded with the likely to have documented chronic obstructive endocrine tumor without lung malignancy).
originally detected radiographic abnormality (Fig. pulmonary disease (COPD) (18%) than those The remaining cases of malignancy were tho-
1). One of the two thoracic radiologists did not inter- without follow-up (7% p < 0.0001). racic metastasis (lung, colon, chondrosarco-
pret or report any of the cases originally. The other ma, head and neck tumor), thoracic involve-
thoracic radiologist only originally reported one of Results of Follow-Up Imaging ment by chronic lymphocytic leukemia, and
the cases. These two radiologists were not blinded The results of follow-up imaging are listed lymphangitic carcinomatosis (breast).
to the outcome. Cytology, surgical pathology, bron- in Tables 3 and 4 and are summarized in the
choscopy, and microbiology results were recorded, flowchart in Figure 2. Other Important Diagnoses
and clinical notes were reviewed. In addition to newly diagnosed malignan-
Malignancy Discovered During Follow-Up cy, 23 patients had important nonmalignant
Statistical Analysis In total, 15 cases of previously undiagnosed diagnoses made on follow-up imaging. Tu-
Statistical analysis was performed using Prism cancer or previously unknown recurrent ma- berculosis or atypical mycobacterial infection
6 (GraphPad Software). Differences in charac- lignancy were found in the study group dur- (n = 6), fungal infection (n = 5), organizing
teristics between patient groups were assessed ing follow-up imaging. Nine of these malig- or eosinophilic pneumonia (n = 5), rounded
for statistical significance using the Fisher exact nancies corresponded with the abnormality on atelectasis (n = 3), alveolar hemorrhage (n =
test. Calculations of significance for mean age be- the index radiograph. Of these nine patients, 1), lung abscess (n = 1), Pneumocystis jiroveci
tween groups were performed using a two-sample eight had a new diagnosis or a new recurrence (n = 1), and septic emboli (n = 1) were among
unequal variance Student t test. A p value of less of non–small cell lung cancer. One patient had the diagnoses made that corresponded with
than 0.05 was considered statistically significant. large B cell lymphoma. On chest radiography, the original chest radiographic abnormali-
only one of nine cases of malignancy was de- ty. The mean age of these 23 patients was 56
Results scribed as a nodule. The remaining eight cases years (median, 58 years; range, 23–83 years).
Study Population and Description of were described as an opacity or consolidation.
Index Abnormalities On chest CT for these nine patients, seven had Time to Follow-Up Imaging
In 2008, 29,138 outpatient chest radiogra- nodules, two had masses not causing lobar or The mean time to first follow-up imaging
phy examinations were performed at our ac- segmental atelectasis, two had consolidation, (radiography or CT) was 80 days (median, 39
ademic center. The reports of 2996 of these and one had a mass with associated right mid- days; range, 0–689 days). The average time
examinations matched the initial screen for dle and lower lobe atelectasis. between index radiography and CT, if per-
recommendations. Our study group includ- The mean age of these nine patients was formed, was 78 days (median, 41 days; range,
ed 805 consecutive reports that were found 68.4 years (median, 73 years; range, 47–83 1–656 days). In eight of nine patients with
to include a recommendation for “radio- years). Five of the nine had a history of ma- newly detected malignancy corresponding
graphic follow-up to resolution” of suspect- lignancy at the time of the index radiogra- with the radiographic abnormality, the mean
ed pneumonia. The patients ranged in age
from 20 to 98 years (424 women, 381 men; TABLE 3:  Modality of Follow-Up and Time to Follow-Up (n = 805)
mean age, 61 years; median, 62 years); 125 Characteristic Value
(16%) of these patients were current smok-
Any follow-up imaging 618 (77)
ers. The most common indications for the
original chest radiography were cough (611, No follow-up imaging 187 (23)
76%), fever (314, 39%), chest pain (142, Follow-up radiography only 432 (53.6)
18%), dyspnea (99, 12%), and wheezing Follow-up radiography and CT 141 (17.5)
(40, 5%). Other demographic and clinical
Follow-up CT only 45 (5.6)
data are summarized in Table 1. The origi-
nal descriptions of index abnormalities are Patients with > 1 follow-up radiography study 185 (23)
summarized in Table 2. Mean time to any first follow-up study 80 d (median, 39 d; range, 0–689 d)
Six hundred eighteen of 805 (77%) patients Mean time to first follow-up radiography 78 d (median, 41 d; range, 0–689 d)
for whom follow-up radiography was recom-
Mean time to first follow-up CT 78 d (median, 41 d; range, 0–656 d)
mended underwent documented follow-up
imaging (285 men and 333 women). One hun- Patients with first follow-up within 90 d 480/618 (60)
dred eighty-eight (23%) patients underwent Note—Except where indicated otherwise, data in parentheses are percentages.

56 AJR:202, January 2014


Radiographic Follow-Up of Pneumonia

Fig. 1—63-year-old woman with 3–4 day history of


productive cough, fever, and pleuritic chest pain.
A and B, Initial posteroanterior (A) and lateral (B)
chest radiographs were interpreted as lingular
pneumonia (arrows) and small left pleural effusion.
Follow-up chest radiography was recommended to
ensure clearance.
C and D, Follow-up posteroanterior (C) and lateral
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(D) chest radiographs obtained 7 weeks later to


ensure clearing of pneumonia (with improved clinical
symptoms) show incomplete clearing of lingular
opacity (arrows) and enlargement of left hilum. Chest
CT was recommended.
E and F, Axial contrast-enhanced CT images of chest
obtained 2 days later in lung (E) and mediastinal
(F) windows show atelectasis in lingula (arrow, E)
and central non–small cell lung cancer obstructing
lingular bronchi (arrow, F).

A B

C D

E F

AJR:202, January 2014 57


Little et al.

TABLE 4:  Important Diagnoses Other Than Pneumonia Corresponding With time to first follow-up imaging (radiography
Radiographic Abnormality or CT) was 17.9 days (median, 16 days; range,
Diagnosis No of Patients 6–31 days). Only one patient had a significant
delay, with follow-up radiography performed
Malignancy 9 186 days after the index study, CT performed
Non–small cell lung cancer 8 2 days subsequent to follow-up radiogra-
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Large B cell lymphoma 1 phy, and an eventual diagnosis of moderate-


ly differentiated lung adenocarcinoma, corre-
Important benign diagnoses 23
sponding with the original abnormality. For
Tuberculosis/atypical mycobacterial infection 6 the 23 patients with important nonmalignant
Eosinophilic or organizing pneumonia 5 diagnoses corresponding with the radiograph-
Fungal infection 5 ic abnormality, the mean time to first follow-
up imaging (radiography or CT) was 70 days
Round atelectasis 3
(median, 8 days; range, 0–366 days).
Abscess 1
Alveolar hemorrhage 1 Discussion
Pneumocystis pneumonia 1 Thoracic malignancy, atypical infection,
and other nonmalignant pulmonary diseases
Septic emboli 1
may appear similar to community-acquired
pneumonia on chest radiography [6–8]. Al-
Patients who underwent follow-up imaging though practice varies, many clinicians and
618/805 (77%) radiologists recommend follow-up chest radi-
ography to confirm clearing of a radiograph-
ic opacity suspected to represent community-
Initial radiographic follow-up CT follow-up only
573/618 (92.7%) 45/618 (7.3%) acquired pneumonia [5]. The rationale for this
practice is to ensure that the patient’s symp-
toms and radiographic findings are in fact due
Persistence or Complete Persistence or Resolution of abnormality or to community-acquired pneumonia rather than
worsening resolution worsening nothing corresponding with another disease. The purpose of this study was
abnormality 396/573 (69.1%) abnormality index chest radiograph
177/573 (30.9%) 13/45 (28.9%) 37/45 (71.1%)
to investigate the outcome of recommendations
for follow-up chest radiography in patients with
a pulmonary opacity initially thought to repre-
Cancer matching Important benign Other incidental sent community-acquired pneumonia.
abnormality diagnosis abnormality Prior research investigating the radio-
1/13 (7.7%) round atelectasis 2 8/13 (61.5%) graphic follow-up of patients diagnosed with
fungal infection 2
4/13 (30.8%) pneumonia has focused on lung cancer as the
primary outcome. These studies show a wide
range (0.4–9.2%) in the incidence of cancer
No chest CT Chest CT performed in patients diagnosed with pneumonia [9–14].
90/177 (50.8%) 87/177 (49.2%)
The most recent study of 3398 patients in Ed-
monton, Alberta, Canada, found a lung cancer
incidence of 2.5% within a subgroup of 1354
Lost to follow-up Cancer matching
89/90 (98.9%) chest radiography patients who underwent chest radiography at
abnormality 90 days [13]. The highest rate of lung can-
1/90 (1.1%)
cer was found in a study by Mortensen et al.
[14] at 9.2%. This high incidence of lung can-
Cancer not matching Cancer matching Important benign Other cer compared with other studies may be due
chest radiography chest radiography diagnosis incidental to the characteristics of the population stud-
abnormality abnormality tuberculosis/atypical abnormality
6/87 (6.9%) 7/87 (8%) mycobacteria 6 55/87 (63.2%)
ied: patients of a Veterans Affairs institution,
eosinophilic/organizing more than 65 years old, inpatients, and pre-
pneumonia 5
fungal infection 3 dominantly men. These prior studies docu-
pneumocystitis 1 ment the epidemiologic association of pneu-
abscess 1 monia and lung cancer but do not specifically
septic emboli 1
alveolar hemorrhage 1 show that the chest radiograph opacity corre-
round atelectasis 1 lated directly with the lung cancer or was a di-
19/87 (23.8%) rect effect of the lung cancer itself.
In our study, we found nine patients (1.5%)
Fig. 2—Flowchart shows outcome of patients who underwent follow-up imaging. in whom a malignancy directly corresponded

58 AJR:202, January 2014


with the index chest radiographic abnormali- chest radiography for suspected community alternative diagnoses may depend on the use
Radiographic Follow-Up of Pneumonia
ty initially suspected to represent pneumonia. acquired pneumonia allowed the detection of of radiographic follow-up.
Our 1.5% incidence of malignancy (not ini- an alternative clinically significant disease in a
tially suspected to be neoplasm on chest ra- total of 32 patients (5%). References
diography) is similar to that found by Wood- A limitation of our study is that we were not 1. Ramsdell J, Narsavage GL, Fink JB. Management
head et al. [12] (1.7%) and Bochud et al. [10] able to achieve 100% compliance for follow-up of community-acquired pneumonia in the home:
(1.2%). Although Tang et al. [13] found a radiography. Our compliance for follow-up im- an American College of Chest Physicians clinical
higher rate of lung malignancy (2.5%), they aging was 60% at 90 days; overall, 77% of pa- position statement. Chest 2005; 127:1752–1763
included all cases of lung cancer whereas our tients received follow-up imaging. This com- 2. Lim WS, Baudouin SV, George RC, et al. BTS
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1.5% incidence of malignancy excludes pa- pares favorably with a recent study by Tang et guidelines for the management of community ac-
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We found that most patients diagnosed Other limitations of our study include the 4. Niederman MS, Mandell LA, Anzueto A, et al.;
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AJR:202, January 2014 59