- Email: [email protected]
Detection failure rate of chest radiography for the identification of nursing and healthcare-associated pneumonia
J Infect Chemother 21 (2015) 492e496
Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Original article
Detection failure rate of chest radiography for the identification of nursing and healthcare-associated pneumonia Naoyuki Miyashita a, *, Yasuhiro Kawai a, Takaaki Tanaka b, Hiroto Akaike b, Hideto Teranishi b, Tokio Wakabayashi b, Takashi Nakano b, Kazunobu Ouchi b, Niro Okimoto a a b
Department of Internal Medicine I, Kawasaki Medical School, Okayama, Japan Department of Pediatrics, Kawasaki Medical School, Okayama, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 December 2014 Received in revised form 5 February 2015 Accepted 4 March 2015 Available online 12 March 2015
Aim: To clarify the detection failure rate of chest radiography for the identification of nursing and healthcare-associated pneumonia (NHCAP), we compared high-resolution computed tomography (HRCT) with chest radiography simultaneously for patients with clinical symptoms and signs leading to a suspicion of NHCAP. Methods: We analyzed 208 NHCAP cases and compared them based on four groups defined using NHCAP criteria, patients who were: Group A) resident in an extended care facility or nursing home; Group B) discharged from a hospital within the preceding 90 days; Group C) receiving nursing care and had poor performance status; and Group D) receiving regular endovascular treatment. Results: Chest radiography was inferior to HRCT for the identification of pneumonia (149 vs 208 cases, p < 0.0001). Among the designated NHCAP criteria, chest radiography identified pneumonia cases at a significantly lower frequency than HRCT in Group A (70 vs 97 cases, p ¼ 0.0190) and Group C (86 vs 136 cases, p < 0.0001). The detection failure rate of chest radiography differed among NHCAP criteria; 27.8% in Group A, 26.5% in Group B, 36.7% in Group C and 5.8% in Group D. Cerebrovascular disease and poor functional status were significantly more frequent in patients in Groups A and C compared with those in Groups B and D. Conclusions: Physicians may underestimate pneumonia shadow in chest radiographs in patients with NHCAP, and the detection failure rate of chest radiography differed among NHCAP criteria. Poor functional status may correlate with the low accuracy of chest radiography in diagnosing pneumonia. © 2015, Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Nursing and healthcare-associated pneumonia Detection failure rate Chest radiograph High-resolution computed tomography Performance status Aspiration
1. Introduction Pneumonia remains a significant cause of morbidity and death worldwide despite the availability of potent antibiotic therapies. In Japan, pneumonia is the third leading cause of mortality. Because 97% of patients who die due to pneumonia are elderly (65 years old), the Japan Respiratory Society (JRS) Guidelines documented a new pneumonia category e nursing and healthcare-associated pneumonia (NHCAP). This category is distinct from community* Corresponding author. Department of Internal Medicine I, Kawasaki Medical School, 2-1-80 Nakasange, Kita-ku, Okayama 700-8505, Japan. Tel.: þ81 86 225 2111; fax: þ81 86 232 8343. E-mail address: [email protected] (N. Miyashita).
acquired pneumonia (CAP) and is relevant to the Japanese population, the Japanese healthcare insurance system, including the nursing-care insurance system, and the pattern of drug-resistant pathogens [1]. Among NHCAP patients, elderly patients who are receiving nursing care with an Eastern Cooperative Oncology Group performance status (PS) of 3 (capable of only limited selfcare, confined to bed or a chair for more than 50% of waking hours) or 4 (completely disabled, unable to carry out any selfcare, totally confined to bed or a chair) [2] were more often seen in hospitals [3e8]. The most frequent cause of NHCAP in Japanese people is thought to be aspiration pneumonia [3e11], which is associated with poor outcomes [3,5,10]. Patients with NHCAP often show a lack of respiratory symptoms such as cough, productive sputum, dyspnea, or chest pain [3].
http://dx.doi.org/10.1016/j.jiac.2015.03.002 1341-321X/© 2015, Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496
Frequently, family members or staff of the long-term care facility bring patients with NHCAP to the Emergency Room owing to melancholy, mental change, loss of appetite, or fever [3]. Chest radiography is regarded as essential to confirm the diagnosis. If physicians cannot detect any abnormal shadow by chest radiography, patients often receive a different diagnosis, which may lead to inadequate therapy. However, there are no data on the frequency that physicians underestimate pneumonia shadows in chest radiography. To clarify the detection failure rate of chest radiography in the identification of NHCAP, we compared high-resolution computed tomography (HRCT) with chest radiography simultaneously for patients with clinical symptoms and signs leading to a suspicion of NHCAP. 2. Patients and methods 2.1. Study populations Patients with clinical signs and symptoms indicative of NHCAP (mental change, loss of appetite, nausea/vomiting, fever, cough, productive sputum, dyspnea, chest pain, hypoxemia or abnormal breath sounds) who visited Kawasaki Medical School, Kawasaki Hospital from January 2013 to September 2014 were enrolled in this study. NHCAP was defined as pneumonia acquired in the community with one or more of the following risk factors according to the JRS guidelines [1]: Group A) pneumonia diagnosed in a resident of an extended care facility or nursing home; Group B) pneumonia diagnosed in a person who had been discharged from a hospital within the preceding 90 days; Group C) pneumonia diagnosed in an elderly or disabled person who was receiving nursing care with PS of 3 or 4; Group D) pneumonia diagnosed in a person who was receiving regular endovascular treatment as an outpatient (dialysis, antibiotic therapy, chemotherapy or immunosuppressant therapy). All cases of pneumonia occurring more than 3 days after hospitalization were considered nosocomial. Informed consent was obtained from all patients, and the study protocol was approved by the Ethics Committee of Kawasaki Medical School. 2.2. Definitions Aspiration pneumonia was defined in accordance with the Japanese Study Group on Aspiration Pulmonary Disease e pneumonia in a patient with a predisposition to aspiration because of dysphagia or swallowing disorders. Swallowing function was assessed using the water swallowing test, repetitive saliva swallowing test, simple-swallowing provocation test, and video fluorography [1,12]. When swallowing function was not assessed using these examinations, the presence of overt symptoms of dysphagia or a medical history of aspiration was determined as a swallowing disorder in the patient. The severity of pneumonia was evaluated using predictive rules in accordance with the respective 5-point scoring systems for CAP in Japan proposed by the JRS e A-DROP (age, dehydration, respiratory failure, orientation disturbance, and low blood pressure) [13]. Microbiological tests, such as Gram stain, cultures, urinary antigen tests, and serological tests, were performed as described previously [3,14]. The microbial etiology was classified as “definitive”, “presumptive” or “unknown”, as reported previously [3,14]. 2.3. Evaluation of radiologic findings At the initial visit, all patients underwent a postero-anterior view and HRCT in a supine position during suspended end inspiration. Chest HRCT examinations were performed using an Aquilion
493
16 (Toshiba Medical Systems, Tochigi, Japan) with 1-mm collimation at 10-mm intervals. Images were obtained at lung parenchyma (level 700 HU; width, 1500 HU) and mediastinal (level 10 HU; width, 300 HU) levels. The time between clinical onset of pneumonia and radiographic examination ranged from 1 to 8 days (mean, 4.5 days). Two observers (radiologists with 36- and 24-years experience, respectively) were blinded to the severity of symptoms as well as to findings obtained from the physical and laboratory examinations. They independently assessed the presence of opacity, loss of vascular marking, nodules, bronchial wall thickening, pleural effusion, and silhouette signs on chest radiographs, and consolidation, ground-glass attenuation, nodules, thickening of the bronchial wall, reticular or linear opacity, and pleural effusion on chest HRCT. The observers also evaluated if the pneumonia was unilateral or bilateral and identified the opacity pattern of pneumonia. Consolidation was defined as air-space opacification with obscuration of the underlying vasculature. Ground-glass attenuation was defined as mildly increased attenuation without obscuration of the underlying vasculature. On chest radiographs, these two patterns were grouped together as opacity or loss of vascular markings. A centrilobular nodule was defined as a nodule identified around the peripheral pulmonary arterial branches or 3e5 mm away from the pleura, interlobular septa, or pulmonary veins. Bronchial wall thickening was defined as thickening identified over widespread areas not close to areas of ground-glass attenuation and/or consolidation. Interlobular septa thickening, intralobular interstitial thickening, and areas of irregular linear opacity were all classified as reticular or linear opacity. A reticular framework in ground-glass attenuation that was described as having a crazypaving appearance was not classified as an area of reticular or linear opacity. The final decisions on the presence of each finding and the opacity pattern for each case were reached by consensus of the two radiologists. In addition, these cases were classified into the following pneumonia patterns by HRCT: lobar pneumonia, bronchopneumonia, bronchitis, or pneumonia with interstitial changes. Lobar pneumonia (air-space pneumonia) was defined as non-segmental pneumonia showing homogenous consolidation that was relatively sharply demarcated from adjacent uninvolved parenchyma. The larger bronchi often remained intact and contained air. Bronchopneumonia was defined as pneumonia that had focal, peripheral, and peribronchiolar consolidation involving one or more segments of a single or several lobes. Consolidation involving the terminal and respiratory bronchioles, and adjacent alveoli, resulted in poorly defined centrilobular nodular opacities measuring 4e10 mm in diameter, or might extend to involve the entire secondary lobe. Bronchiolitis was defined as disease that showed a pattern of small centrilobular nodules and branching lines as a result of inflammation of the bronchiolar wall, and filling of the bronchiolar lumen by exudate. Pneumonia with interstitial changes had either a reticular or reticulonodular pattern. 2.4. Statistical analysis Statistical analysis was performed using Stat View version 5.0. (SAS Institute Inc, Cary, NC, USA). The incidences of underlying conditions, clinical findings, and radiographic findings were analyzed using Fisher's Exact test. Mean age of patients and laboratory data were compared using Student's t test. For each radiological finding, kappa values were calculated between the observers. The evaluation of kappa as a measure of interobserver ratios was as follows: 0.01e0.19, poor agreement; 0.20e0.39, fair; 0.40e0.59, moderate; 0.60e0.79, substantial; and 0.80e1.00, almost perfect [15].
494
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496
Table 1 Characteristics of 208 patients with nursing and healthcare associated pneumonia (NHCAP).a Characteristic
NHCAP patients
Group A: Pneumonia diagnosed in a resident of an extended care facility or nursing home Group B: Pneumonia diagnosed in a person who has been discharged from a hospital within the preceding 90 days Group C: Pneumonia diagnosed in an elderly or disabled person who is receiving nursing care with an Eastern Cooperative Oncology Group performance status of 3 or 4 Group D: Pneumonia diagnosed in a person who is receiving regular endovascular treatment as an outpatient (dialysis, antibiotic therapy, chemotherapy, immunosuppressant therapy)
97 (46) 79 (38)
136 (65)
17 (8)
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
3. Results 3.1. Patient characteristics During the study period, we enrolled and analyzed 318 patients with suspected NHCAP, and the total number of patients who were scored as having pneumonia-related lesions was 208 (65%). Among the NHCAP criteria, patients with pneumonia diagnosed in an elderly or disabled person who was receiving nursing care with a PS of 3 or 4 were most often seen in our study (Table 1). Ninety-five patients (45%) had overlapping NHCAP criteria. The characteristics of NHCAP patients in each group are shown in Table 2. Among the 17 patients in Group D, 13 patients (76%) were receiving regular hemodialysis for chronic renal failure. NHCAP patients in Groups A, B, and C were significantly older than those in Group D (82.1, 80.9, and 82.5 years-old vs 69.8 years-old, respectively, p < 0.0001). Among co-morbid conditions, cerebrovascular disease was significantly more frequently in patients in Groups A and C compared with those with Groups B and D (Table 2, p < 0.0001). Among general conditions, patients with poor functional status (PS grade 3 and 4) were more frequent in Groups A and C than in Groups B and D (Table 2, p < 0.0001). Table 2 Clinical characteristics of 208 patients with nursing and healthcare-associated pneumonia in an each groupa. Characteristics
Group A
Group B
Group C
Group D
Numbera Age, mean ± SD (years) Male: Female Co-morbid conditionsa Cerebrovascular disease Chronic lung disease Chronic heart disease Diabetes mellitus Chronic renal disease Neoplastic disease Chronic liver disease Autoimmune disease Performance status grade 3a Probable aspiration
97 82.1 ± 9.1 49: 48
79 80.9 ± 9.4 50: 29
136 82.5 ± 9.0 75: 61
17 69.8 ± 6.9 16: 1
65 (67) 15 (15) 6 (6) 10 (10) 9 (9) 1 (1) 2 (2) 2 (2) 73 (75) 70 (72)
26 (33) 33 (41) 8 (10) 16 (20) 5 (6) 3 (3) 0 2 (2) 44 (55) 44 (55)
81 (59) 21 (15) 6 (4) 16 (11) 6 (4) 7 (5) 1 (7) 5 (3) 136 (100) 103 (75)
2 (11) 8 (47) 1 (5) 5 (29) 13 (76) 2 (11) 1 (5) 0 0 0
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
Table 3 Prevalence of pneumonia diagnosed by chest radiography or high-resolution computed tomography (HRCT) for 318 patients with suspected nursing and healthcare associated pneumonia. Variable
No. (%) diagnosed by chest radiography
No. (%) diagnosed by HRCT
p-Value
Group Aa Group Ba Group Ca Group Da All patients
70 58 86 16 149
97 79 136 17 208
0.0190 0.0535 <0.0001 >0.9999 <0.0001
(22) (18) (27) (5) (46)
(30) (24) (42) (5) (65)
a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
3.2. Radiographic findings The kappa value between the two readers was 0.832 for chest radiographs and 0.736 for HRCT. Table 3 shows that chest radiography identified pneumonia cases at a significantly lower rate than HRCT (149 cases vs 208 cases, respectively; p < 0.0001). When the results of the two methods were obtained, HRCT identified all 149 NHCAP cases that were revealed by chest radiography. Among the NHCAP criteria, chest radiography identified pneumonia cases less often than HRCT in Group A (70 cases vs 97 cases, p ¼ 0.0190) and Group C (86 cases vs 136 cases, p < 0.0001). Table 4 summarizes the radiologic findings. The proportion of each radiologic findings did not differ among the four groups. 3.3. Affected lung lobes and pattern of pneumonia Table 5 shows a comparison of the affected lung lobes visualized with HRCT in each group. Bilateral infiltrates were more often seen in all groups, and most infiltrates were located in the lower lobes in all groups. At the segment level, posterior basal segments of both lower lobes were often undiagnosed by chest radiography. Table 6 shows a comparison of the types of pneumonia identified by HRCT in each group. The kappa value of HRCT findings between the two observers was 0.797 for the observed patterns of pneumonia. The pattern of pneumonia was identical among patients in Groups A, B, and C and different from patients in Group D. Bronchopneumonia was the most-frequently identified pattern of
Table 4 Chest radiography and high-resolution computed tomography (HRCT) findings in 208 patients with nursing and healthcare associated pneumonia in an each groupa. Parameters
Chest radiography findings Opacity Loss of vascular marking Nodules Bronchial wall thickening Pleural effusion Silhouette sign Chest HRCT findings Air-space consolidation Ground-glass attenuation Nodules Bronchial wall thickening Reticular or linear opacity Pleural effusion
Group A
Group B
Group C
Group D
N ¼ 97
N ¼ 79
N ¼ 136
N ¼ 17
34 45 2 2 8 14
(35) (46) (2) (2) (8) (14)
33 32 3 2 5 9
(41) (40) (3) (2) (6) (11)
45 50 7 4 8 12
(33) (36) (5) (3) (5) (8)
9 (53) 10 (58) 1 (5) 0 1 (5) 0
67 73 28 39 12 58
(69) (75) (28) (40) (12) (59)
47 59 21 27 10 40
(59) (74) (26) (34) (12) (50)
86 102 44 58 17 71
(63) (75) (32) (42) (12) (52)
12 (70) 14 (82) 2 (11) 6 (35) 2 (11) 11 (64)
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496 Table 5 Affected lung lobes visualized using high-resolution computed tomography (HRCT) in 208 patients with nursing and healthcare associated pneumonia in an each groupa. Site of infiltrate
Group A
Group B
Group C
Group D
N ¼ 97
N ¼ 79
N ¼ 136
N ¼ 17
Unilateral Right Upper lobe Middle lobe Lower lobe Left Upper lobe Lingual lobe Lower lobe Bilateral Right Upper lobe Middle lobe Lower lobe Left Upper lobe Lingual lobe Lower lobe
43 (44) 3 5 16 2 4 13 54 (56) 10 10 45 0 9 45
32 (41) 4 4 10 3 2 9 47 (59) 14 7 32 15 8 33
60 (44) 4 4 25 4 3 20 76 (56) 11 13 58 11 10 61
8 (47) 1 1 2 1 1 2 9 (53) 3 2 6 3 2 6
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
pneumonia in patients in Groups A, B, and C. Lobar pneumonia was more often seen in patients in Group D than in patients in the other groups. 3.4. Relationship of chest radiography and HRCT with pneumonia severity and pathogens Pneumonia severity was classified by means of the A-DROP system of the JRS as follows: mild, 11 patients (5%); moderate, 103 patients (49%); severe, 68 patients (32%); and very severe, 26 patients (12%). Among the pneumonia severity groups, chest radiography identified pneumonia cases significantly less often than HRCT in the moderate group (67 cases vs 103 cases, p ¼ 0.0171) (Table 7). Among NHCAP patients, the most common pathogens were Streptococcus pneumoniae (19%) followed by Staphylococcus aureus (11%), Klebsiella species (9%), Pseudomonas aeruginosa (5%), Haemophilus influenzae (4%), and Moraxella catarrhalis (1%). The detection failure rate of chest radiography was not different between pathogens. 4. Discussion Usually, chest radiography is the first imaging technique utilized for the evaluation of acute respiratory symptoms, and this method
Table 6 Pattern of pneumonia diagnosed by high-resolution computed tomography (HRCT) in 208 patients with nursing and healthcare associated pneumonia in an each groupa. Pattern of pneumonia
Lobar pneumonia Bronchopneumonia Bronchiolitis Pneumonia with interstitial changes
Group A
Group B
Group C
Group D
N ¼ 97
N ¼ 79
N ¼ 136
N ¼ 17
18 72 6 1
13 59 4 3
22 101 12 1
7 7 1 2
(18) (74) (9) (1)
(16) (74) (5) (3)
(16) (74) (8) (0.7)
(41) (41) (5) (11)
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
495
Table 7 Prevalence of pneumonia diagnosed by chest radiography or high-resolution computed tomography (HRCT) in 318 patients with suspected nursing and healthcare associated pneumonia. Pneumonia severitya
No. (%) diagnosed by chest radiography
No. (%) diagnosed by HRCT
p-Value
Mild Moderate Severe Very severe All patients
6 67 50 26 149
11 103 68 26 208
0.3257 0.0171 0.0826 >0.9999 <0.0001
(2) (21) (15) (8) (46)
(3) (32) (21) (8) (65)
a Pneumonia severity was classified by means of the A-DROP systems of the Japan Respiratory Society.
is still recommended as the standard reference method for confirming the diagnosis of pneumonia [1,13]. Some reports have indicated that CT images can more accurately provide detailed information about the lung parenchyma than a routine chest radiograph [16e18]. In this study, we found that pneumonia shadows were not detected by chest radiography in 59 (28.3%) out of 208 NHCAP patients. The detection failure rate of chest radiography was different among NHCAP criteria; 27.8% in Group A, 26.5% in Group B, 36.7% in Group C, and 5.8% in Group D. Chest radiography identified pneumonia cases at significantly lower rates than HRCT in Group A and Group C (Table 3). The most important difference between Groups A and C and Groups B and D was the frequency of poor functional status (PS grade 3 or 4) mainly owing to cerebrovascular disease. Thus, we believe that poor functional status may correlate with the low accuracy of chest radiography in diagnosing pneumonia. There have been some previous reports that assessed the diagnostic value of chest radiography for the identification of pneumonia in different types of respiratory tract infections. In a study of CAP, Syrjala et al. demonstrated that HRCT was superior to chest radiography for the identification of pneumonia (26 cases versus 18 cases; p ¼ 0.04) [16]. Pneumonia shadows were not detected by chest radiography in 8 (30.7%) out of 26 CAP patients. The same group also demonstrated that HRCT is more sensitive than radiography in detecting lower respiratory tract infectionrelated lung lesions in a primary care population [17]. Lower respiratory tract infection-related lung lesions were not detected by chest radiography in 8 (42.1%) out of 19 CAP patients. Although there were small numbers of patients in these study groups, the detection failure rate of chest radiography in CAP patients was higher than in our NHCAP study. To clarify the difference in CAP and NHCAP in terms of detection capability, a comparative study with CAP and NHCAP patients is needed. Chest CT studies in patients with aspiration pneumonia (classified as NHCAP and poor functional status) demonstrated that the lung opacities were distributed in the posterior lung fields and in the lower zone, and there was no anterior- or upper-predominant distribution [11]. In bedridden patients (classified as NHCAP and poor functional status), obtaining a lateral view is impossible, and the dome of the diaphragm may project over a significant portion of the lower zone. Thus, it may be difficult to interpret chest radiographs from patients with NHCAP, especially in patients with poor functional status [18]. Physicians should pay careful attention to the presence of pneumonia in patients with normal chest radiographic findings who have poor functional status. Diffuse aspiration panbronchiolitis (DAB) is a type of aspiration pneumonia that is characterized by chronic inflammation of bronchioles caused by recurrent aspiration of foreign particles in elderly patients [19,20]. Radiographically and pathologically at autopsy, DAB resembled diffuse panbronchiolitis [21]. The incidence of DAB in a total of 4880 autopsy cases was 0.64%, and 70% of
496
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496
patients with DAB were bedridden [19]. In our study, 18 (8%) of 208 NHCAP patients showed a radiographic pattern consistent with DAB. Thus, DAB is not a rare type among patients with NHCAP. There has been controversy regarding the benefit of chest CT for diagnostic purposes in general and because of the radiation risk in particular. However, Japanese physicians frequently use chest CT to assess patients suspected as having pneumonia, possibly because the healthcare insurance system in Japan allows clinicians to carry out CT. The benefit obtained with the use of HRCT may compensate for the higher cost in situations where a confident and prompt diagnosis is desirable. Further studies are needed to formulate costeffective recommendations. In conclusion, our results indicated that physicians often underestimate the pneumonia shadow in chest radiography in patients with NHCAP and the detection failure rate of chest radiography was different among NHCAP criteria. Poor functional status may correlate with the low accuracy of chest radiography in diagnosing pneumonia. Conflict of interest All of the authors have explicitly stated that there are no conflicts of interest in connection with this article. Acknowledgments This study was supported in part by MEXT KAKENHI (19591190 and 21591304) and Project Research Grants from Kawasaki Medical School (13-401, 14-402, 15-405A, 16-405M, 17-402M, 18-401, 19402M, 204030). References [1] Kohno S, Imamura Y, Shindo Y, Seki M, Ishida T, Teramoto S, et al. Clinical practice guidelines for nursing- and healthcare-associated pneumonia (NHCAP) [complete translation]. Respir Investig 2014;51:103e26. [2] Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 1982;5:649e55. [3] Miyashita N, Kawai Y, Akaike H, Yamaguchi T, Ouchi K, Hayashi T, et al. Clinical features and the role of atypical pathogens in nursing and healthcare-associated pneumonia (NHCAP): differences between teaching university hospital and community hospital. Intern Med 2012;51:585e94. [4] Ishida T, Tachibana H, Ito A, Yoshioka H, Arita M, Hashimoto T. Clinical characteristics of nursing and healthcare-associated pneumonia: a Japanese variant of healthcare-associated pneumonia. Intern Med 2012;51:2537e44.
[5] Fukuyama H, Yamashiro S, Tamaki H, Kishaba T. A prospective comparison of nursing- and healthcare-associated pneumonia (NHCAP) with communityacquired pneumonia (CAP). J Infect Chemother 2013;19:719e26. [6] Oshitani Y, Nagai H, Matsui H, Aoshima M. Reevaluation of the Japanese guideline for healthcare-associated pneumonia in a medium-size community hospital in Japan. J Infect Chemother 2013;19:579e87. [7] Kaku N, Yanagihara K, Morinaga Y, Izumikawa K, Nagashima S, Kakeya H, et al. The definition of healthcare-associated pneumonia (HCAP) is insufficient for the medical environment in Japan: a comparison of HCAP and nursing and healthcare-associated pneumonia (NHCAP). J Infect Chemother 2013;19: 70e6. [8] Nakagawa N, Saiato Y, Sasaki M, Tsuda Y, Mochizuki H, Takahashi H. Comparison of clinical profile in elderly patients with nursing and healthcareassociated pneumonia, and those with community-acquired pneumonia. Geriatr Gerontol Int 2014;14:362e71. [9] Teramoto S, Fukuchi Y, Sasaki H, Sato K, Sekizawa K, Matsuse T. High incidence of aspiration pneumonia in community and hospital acquired pneumonia in hospitalized patients: a multicenter, prospective study in Japan. J Am Geriatr Soc 2008;56:577e9. [10] Komiya K, Ishii H, Umeki K, Mizunoe S, Okada F, Johkoh T, et al. Impact of aspiration pneumonia in patients with community-acquired pneumonia and healthcare-associated pneumonia: a multicenter retrospective cohort study. Respirology 2013;18:514e21. [11] Komiya K, Ishii H, Umeki K, Kawamura T, Okada F, Okabe E, et al. Computed tomography findings of aspiration pneumonia in 53 patients. Geriatr Gerontol Int 2013;13:580e5. [12] The Committee for the Japanese Respiratory Society Guidelines in Management of Respiratory Infections. The Japanese Respiratory Society guideline for the management of hospital-acquired pneumonia in adults. Respirology 2008;14:S1e71. [13] The Committee for the Japanese Respiratory Society Guidelines in Management of Respiratory Infections. The Japanese Respiratory Society guideline for the management of community-acquired pneumonia in adults. Respirology 2006;11:S1e133. [14] Miyashita N, Kawai Y, Yamaguchi T, Ouchi K, Oka M, the Atypical Pathogen Study Group. Clinical potential of diagnostic methods for the rapid diagnosis of Mycoplasma pneumoniae pneumonia in adults. Eur J Clin Microbiol Infect Dis 2011;30:439e46. [15] Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159e74. [16] Syrjala H, Broas M, Suramo I, Ojala A, Lahde S. High-resolution computed tomography for the diagnosis of community-acquired pneumonia. Clin Infect Dis 1998;27:358e63. [17] Lahde S, Jartti A, Broas M, Koivisto M, Syrjala H. HRCT findings in the lungs of primary care patients with lower respiratory tract infection. Acta Radiol 2002;43:159e63. [18] Esayag Y, Nikitin I, Bar-Ziv J, Cytter R, Hadas-Halpern I, Zalut T, et al. Diagnostic value of chest radiographs in bedridden patients suspected of having pneumonia. Am J Med 2010;123. 88.e1e6. [19] Matsuse T, Oka T, Kida K, Fukuchi Y. Importance of diffuse aspiration bronchiolitis caused by chronic occult aspiration in the elderly. Chest 1996;110: 1289e93. [20] Matsuse T, Teramoto S, Matsui H, Ouchi Y, Fukuchi Y. Widespread occurrence of diffuse aspiration bronchitis in patients with dysphagia, irrespective of age. Chest 1998;114:350e1. [21] Homma H, Yamanaka A, Tanimoto S, Tamura M, Chijimatsu Y, Kira S, et al. Diffuse panbronchiolitis: a disease of the transitional zone of the lung. Chest 1983;83:63e9.
Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Original article
Detection failure rate of chest radiography for the identification of nursing and healthcare-associated pneumonia Naoyuki Miyashita a, *, Yasuhiro Kawai a, Takaaki Tanaka b, Hiroto Akaike b, Hideto Teranishi b, Tokio Wakabayashi b, Takashi Nakano b, Kazunobu Ouchi b, Niro Okimoto a a b
Department of Internal Medicine I, Kawasaki Medical School, Okayama, Japan Department of Pediatrics, Kawasaki Medical School, Okayama, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 December 2014 Received in revised form 5 February 2015 Accepted 4 March 2015 Available online 12 March 2015
Aim: To clarify the detection failure rate of chest radiography for the identification of nursing and healthcare-associated pneumonia (NHCAP), we compared high-resolution computed tomography (HRCT) with chest radiography simultaneously for patients with clinical symptoms and signs leading to a suspicion of NHCAP. Methods: We analyzed 208 NHCAP cases and compared them based on four groups defined using NHCAP criteria, patients who were: Group A) resident in an extended care facility or nursing home; Group B) discharged from a hospital within the preceding 90 days; Group C) receiving nursing care and had poor performance status; and Group D) receiving regular endovascular treatment. Results: Chest radiography was inferior to HRCT for the identification of pneumonia (149 vs 208 cases, p < 0.0001). Among the designated NHCAP criteria, chest radiography identified pneumonia cases at a significantly lower frequency than HRCT in Group A (70 vs 97 cases, p ¼ 0.0190) and Group C (86 vs 136 cases, p < 0.0001). The detection failure rate of chest radiography differed among NHCAP criteria; 27.8% in Group A, 26.5% in Group B, 36.7% in Group C and 5.8% in Group D. Cerebrovascular disease and poor functional status were significantly more frequent in patients in Groups A and C compared with those in Groups B and D. Conclusions: Physicians may underestimate pneumonia shadow in chest radiographs in patients with NHCAP, and the detection failure rate of chest radiography differed among NHCAP criteria. Poor functional status may correlate with the low accuracy of chest radiography in diagnosing pneumonia. © 2015, Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Nursing and healthcare-associated pneumonia Detection failure rate Chest radiograph High-resolution computed tomography Performance status Aspiration
1. Introduction Pneumonia remains a significant cause of morbidity and death worldwide despite the availability of potent antibiotic therapies. In Japan, pneumonia is the third leading cause of mortality. Because 97% of patients who die due to pneumonia are elderly (65 years old), the Japan Respiratory Society (JRS) Guidelines documented a new pneumonia category e nursing and healthcare-associated pneumonia (NHCAP). This category is distinct from community* Corresponding author. Department of Internal Medicine I, Kawasaki Medical School, 2-1-80 Nakasange, Kita-ku, Okayama 700-8505, Japan. Tel.: þ81 86 225 2111; fax: þ81 86 232 8343. E-mail address: [email protected] (N. Miyashita).
acquired pneumonia (CAP) and is relevant to the Japanese population, the Japanese healthcare insurance system, including the nursing-care insurance system, and the pattern of drug-resistant pathogens [1]. Among NHCAP patients, elderly patients who are receiving nursing care with an Eastern Cooperative Oncology Group performance status (PS) of 3 (capable of only limited selfcare, confined to bed or a chair for more than 50% of waking hours) or 4 (completely disabled, unable to carry out any selfcare, totally confined to bed or a chair) [2] were more often seen in hospitals [3e8]. The most frequent cause of NHCAP in Japanese people is thought to be aspiration pneumonia [3e11], which is associated with poor outcomes [3,5,10]. Patients with NHCAP often show a lack of respiratory symptoms such as cough, productive sputum, dyspnea, or chest pain [3].
http://dx.doi.org/10.1016/j.jiac.2015.03.002 1341-321X/© 2015, Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496
Frequently, family members or staff of the long-term care facility bring patients with NHCAP to the Emergency Room owing to melancholy, mental change, loss of appetite, or fever [3]. Chest radiography is regarded as essential to confirm the diagnosis. If physicians cannot detect any abnormal shadow by chest radiography, patients often receive a different diagnosis, which may lead to inadequate therapy. However, there are no data on the frequency that physicians underestimate pneumonia shadows in chest radiography. To clarify the detection failure rate of chest radiography in the identification of NHCAP, we compared high-resolution computed tomography (HRCT) with chest radiography simultaneously for patients with clinical symptoms and signs leading to a suspicion of NHCAP. 2. Patients and methods 2.1. Study populations Patients with clinical signs and symptoms indicative of NHCAP (mental change, loss of appetite, nausea/vomiting, fever, cough, productive sputum, dyspnea, chest pain, hypoxemia or abnormal breath sounds) who visited Kawasaki Medical School, Kawasaki Hospital from January 2013 to September 2014 were enrolled in this study. NHCAP was defined as pneumonia acquired in the community with one or more of the following risk factors according to the JRS guidelines [1]: Group A) pneumonia diagnosed in a resident of an extended care facility or nursing home; Group B) pneumonia diagnosed in a person who had been discharged from a hospital within the preceding 90 days; Group C) pneumonia diagnosed in an elderly or disabled person who was receiving nursing care with PS of 3 or 4; Group D) pneumonia diagnosed in a person who was receiving regular endovascular treatment as an outpatient (dialysis, antibiotic therapy, chemotherapy or immunosuppressant therapy). All cases of pneumonia occurring more than 3 days after hospitalization were considered nosocomial. Informed consent was obtained from all patients, and the study protocol was approved by the Ethics Committee of Kawasaki Medical School. 2.2. Definitions Aspiration pneumonia was defined in accordance with the Japanese Study Group on Aspiration Pulmonary Disease e pneumonia in a patient with a predisposition to aspiration because of dysphagia or swallowing disorders. Swallowing function was assessed using the water swallowing test, repetitive saliva swallowing test, simple-swallowing provocation test, and video fluorography [1,12]. When swallowing function was not assessed using these examinations, the presence of overt symptoms of dysphagia or a medical history of aspiration was determined as a swallowing disorder in the patient. The severity of pneumonia was evaluated using predictive rules in accordance with the respective 5-point scoring systems for CAP in Japan proposed by the JRS e A-DROP (age, dehydration, respiratory failure, orientation disturbance, and low blood pressure) [13]. Microbiological tests, such as Gram stain, cultures, urinary antigen tests, and serological tests, were performed as described previously [3,14]. The microbial etiology was classified as “definitive”, “presumptive” or “unknown”, as reported previously [3,14]. 2.3. Evaluation of radiologic findings At the initial visit, all patients underwent a postero-anterior view and HRCT in a supine position during suspended end inspiration. Chest HRCT examinations were performed using an Aquilion
493
16 (Toshiba Medical Systems, Tochigi, Japan) with 1-mm collimation at 10-mm intervals. Images were obtained at lung parenchyma (level 700 HU; width, 1500 HU) and mediastinal (level 10 HU; width, 300 HU) levels. The time between clinical onset of pneumonia and radiographic examination ranged from 1 to 8 days (mean, 4.5 days). Two observers (radiologists with 36- and 24-years experience, respectively) were blinded to the severity of symptoms as well as to findings obtained from the physical and laboratory examinations. They independently assessed the presence of opacity, loss of vascular marking, nodules, bronchial wall thickening, pleural effusion, and silhouette signs on chest radiographs, and consolidation, ground-glass attenuation, nodules, thickening of the bronchial wall, reticular or linear opacity, and pleural effusion on chest HRCT. The observers also evaluated if the pneumonia was unilateral or bilateral and identified the opacity pattern of pneumonia. Consolidation was defined as air-space opacification with obscuration of the underlying vasculature. Ground-glass attenuation was defined as mildly increased attenuation without obscuration of the underlying vasculature. On chest radiographs, these two patterns were grouped together as opacity or loss of vascular markings. A centrilobular nodule was defined as a nodule identified around the peripheral pulmonary arterial branches or 3e5 mm away from the pleura, interlobular septa, or pulmonary veins. Bronchial wall thickening was defined as thickening identified over widespread areas not close to areas of ground-glass attenuation and/or consolidation. Interlobular septa thickening, intralobular interstitial thickening, and areas of irregular linear opacity were all classified as reticular or linear opacity. A reticular framework in ground-glass attenuation that was described as having a crazypaving appearance was not classified as an area of reticular or linear opacity. The final decisions on the presence of each finding and the opacity pattern for each case were reached by consensus of the two radiologists. In addition, these cases were classified into the following pneumonia patterns by HRCT: lobar pneumonia, bronchopneumonia, bronchitis, or pneumonia with interstitial changes. Lobar pneumonia (air-space pneumonia) was defined as non-segmental pneumonia showing homogenous consolidation that was relatively sharply demarcated from adjacent uninvolved parenchyma. The larger bronchi often remained intact and contained air. Bronchopneumonia was defined as pneumonia that had focal, peripheral, and peribronchiolar consolidation involving one or more segments of a single or several lobes. Consolidation involving the terminal and respiratory bronchioles, and adjacent alveoli, resulted in poorly defined centrilobular nodular opacities measuring 4e10 mm in diameter, or might extend to involve the entire secondary lobe. Bronchiolitis was defined as disease that showed a pattern of small centrilobular nodules and branching lines as a result of inflammation of the bronchiolar wall, and filling of the bronchiolar lumen by exudate. Pneumonia with interstitial changes had either a reticular or reticulonodular pattern. 2.4. Statistical analysis Statistical analysis was performed using Stat View version 5.0. (SAS Institute Inc, Cary, NC, USA). The incidences of underlying conditions, clinical findings, and radiographic findings were analyzed using Fisher's Exact test. Mean age of patients and laboratory data were compared using Student's t test. For each radiological finding, kappa values were calculated between the observers. The evaluation of kappa as a measure of interobserver ratios was as follows: 0.01e0.19, poor agreement; 0.20e0.39, fair; 0.40e0.59, moderate; 0.60e0.79, substantial; and 0.80e1.00, almost perfect [15].
494
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496
Table 1 Characteristics of 208 patients with nursing and healthcare associated pneumonia (NHCAP).a Characteristic
NHCAP patients
Group A: Pneumonia diagnosed in a resident of an extended care facility or nursing home Group B: Pneumonia diagnosed in a person who has been discharged from a hospital within the preceding 90 days Group C: Pneumonia diagnosed in an elderly or disabled person who is receiving nursing care with an Eastern Cooperative Oncology Group performance status of 3 or 4 Group D: Pneumonia diagnosed in a person who is receiving regular endovascular treatment as an outpatient (dialysis, antibiotic therapy, chemotherapy, immunosuppressant therapy)
97 (46) 79 (38)
136 (65)
17 (8)
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
3. Results 3.1. Patient characteristics During the study period, we enrolled and analyzed 318 patients with suspected NHCAP, and the total number of patients who were scored as having pneumonia-related lesions was 208 (65%). Among the NHCAP criteria, patients with pneumonia diagnosed in an elderly or disabled person who was receiving nursing care with a PS of 3 or 4 were most often seen in our study (Table 1). Ninety-five patients (45%) had overlapping NHCAP criteria. The characteristics of NHCAP patients in each group are shown in Table 2. Among the 17 patients in Group D, 13 patients (76%) were receiving regular hemodialysis for chronic renal failure. NHCAP patients in Groups A, B, and C were significantly older than those in Group D (82.1, 80.9, and 82.5 years-old vs 69.8 years-old, respectively, p < 0.0001). Among co-morbid conditions, cerebrovascular disease was significantly more frequently in patients in Groups A and C compared with those with Groups B and D (Table 2, p < 0.0001). Among general conditions, patients with poor functional status (PS grade 3 and 4) were more frequent in Groups A and C than in Groups B and D (Table 2, p < 0.0001). Table 2 Clinical characteristics of 208 patients with nursing and healthcare-associated pneumonia in an each groupa. Characteristics
Group A
Group B
Group C
Group D
Numbera Age, mean ± SD (years) Male: Female Co-morbid conditionsa Cerebrovascular disease Chronic lung disease Chronic heart disease Diabetes mellitus Chronic renal disease Neoplastic disease Chronic liver disease Autoimmune disease Performance status grade 3a Probable aspiration
97 82.1 ± 9.1 49: 48
79 80.9 ± 9.4 50: 29
136 82.5 ± 9.0 75: 61
17 69.8 ± 6.9 16: 1
65 (67) 15 (15) 6 (6) 10 (10) 9 (9) 1 (1) 2 (2) 2 (2) 73 (75) 70 (72)
26 (33) 33 (41) 8 (10) 16 (20) 5 (6) 3 (3) 0 2 (2) 44 (55) 44 (55)
81 (59) 21 (15) 6 (4) 16 (11) 6 (4) 7 (5) 1 (7) 5 (3) 136 (100) 103 (75)
2 (11) 8 (47) 1 (5) 5 (29) 13 (76) 2 (11) 1 (5) 0 0 0
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
Table 3 Prevalence of pneumonia diagnosed by chest radiography or high-resolution computed tomography (HRCT) for 318 patients with suspected nursing and healthcare associated pneumonia. Variable
No. (%) diagnosed by chest radiography
No. (%) diagnosed by HRCT
p-Value
Group Aa Group Ba Group Ca Group Da All patients
70 58 86 16 149
97 79 136 17 208
0.0190 0.0535 <0.0001 >0.9999 <0.0001
(22) (18) (27) (5) (46)
(30) (24) (42) (5) (65)
a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
3.2. Radiographic findings The kappa value between the two readers was 0.832 for chest radiographs and 0.736 for HRCT. Table 3 shows that chest radiography identified pneumonia cases at a significantly lower rate than HRCT (149 cases vs 208 cases, respectively; p < 0.0001). When the results of the two methods were obtained, HRCT identified all 149 NHCAP cases that were revealed by chest radiography. Among the NHCAP criteria, chest radiography identified pneumonia cases less often than HRCT in Group A (70 cases vs 97 cases, p ¼ 0.0190) and Group C (86 cases vs 136 cases, p < 0.0001). Table 4 summarizes the radiologic findings. The proportion of each radiologic findings did not differ among the four groups. 3.3. Affected lung lobes and pattern of pneumonia Table 5 shows a comparison of the affected lung lobes visualized with HRCT in each group. Bilateral infiltrates were more often seen in all groups, and most infiltrates were located in the lower lobes in all groups. At the segment level, posterior basal segments of both lower lobes were often undiagnosed by chest radiography. Table 6 shows a comparison of the types of pneumonia identified by HRCT in each group. The kappa value of HRCT findings between the two observers was 0.797 for the observed patterns of pneumonia. The pattern of pneumonia was identical among patients in Groups A, B, and C and different from patients in Group D. Bronchopneumonia was the most-frequently identified pattern of
Table 4 Chest radiography and high-resolution computed tomography (HRCT) findings in 208 patients with nursing and healthcare associated pneumonia in an each groupa. Parameters
Chest radiography findings Opacity Loss of vascular marking Nodules Bronchial wall thickening Pleural effusion Silhouette sign Chest HRCT findings Air-space consolidation Ground-glass attenuation Nodules Bronchial wall thickening Reticular or linear opacity Pleural effusion
Group A
Group B
Group C
Group D
N ¼ 97
N ¼ 79
N ¼ 136
N ¼ 17
34 45 2 2 8 14
(35) (46) (2) (2) (8) (14)
33 32 3 2 5 9
(41) (40) (3) (2) (6) (11)
45 50 7 4 8 12
(33) (36) (5) (3) (5) (8)
9 (53) 10 (58) 1 (5) 0 1 (5) 0
67 73 28 39 12 58
(69) (75) (28) (40) (12) (59)
47 59 21 27 10 40
(59) (74) (26) (34) (12) (50)
86 102 44 58 17 71
(63) (75) (32) (42) (12) (52)
12 (70) 14 (82) 2 (11) 6 (35) 2 (11) 11 (64)
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496 Table 5 Affected lung lobes visualized using high-resolution computed tomography (HRCT) in 208 patients with nursing and healthcare associated pneumonia in an each groupa. Site of infiltrate
Group A
Group B
Group C
Group D
N ¼ 97
N ¼ 79
N ¼ 136
N ¼ 17
Unilateral Right Upper lobe Middle lobe Lower lobe Left Upper lobe Lingual lobe Lower lobe Bilateral Right Upper lobe Middle lobe Lower lobe Left Upper lobe Lingual lobe Lower lobe
43 (44) 3 5 16 2 4 13 54 (56) 10 10 45 0 9 45
32 (41) 4 4 10 3 2 9 47 (59) 14 7 32 15 8 33
60 (44) 4 4 25 4 3 20 76 (56) 11 13 58 11 10 61
8 (47) 1 1 2 1 1 2 9 (53) 3 2 6 3 2 6
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
pneumonia in patients in Groups A, B, and C. Lobar pneumonia was more often seen in patients in Group D than in patients in the other groups. 3.4. Relationship of chest radiography and HRCT with pneumonia severity and pathogens Pneumonia severity was classified by means of the A-DROP system of the JRS as follows: mild, 11 patients (5%); moderate, 103 patients (49%); severe, 68 patients (32%); and very severe, 26 patients (12%). Among the pneumonia severity groups, chest radiography identified pneumonia cases significantly less often than HRCT in the moderate group (67 cases vs 103 cases, p ¼ 0.0171) (Table 7). Among NHCAP patients, the most common pathogens were Streptococcus pneumoniae (19%) followed by Staphylococcus aureus (11%), Klebsiella species (9%), Pseudomonas aeruginosa (5%), Haemophilus influenzae (4%), and Moraxella catarrhalis (1%). The detection failure rate of chest radiography was not different between pathogens. 4. Discussion Usually, chest radiography is the first imaging technique utilized for the evaluation of acute respiratory symptoms, and this method
Table 6 Pattern of pneumonia diagnosed by high-resolution computed tomography (HRCT) in 208 patients with nursing and healthcare associated pneumonia in an each groupa. Pattern of pneumonia
Lobar pneumonia Bronchopneumonia Bronchiolitis Pneumonia with interstitial changes
Group A
Group B
Group C
Group D
N ¼ 97
N ¼ 79
N ¼ 136
N ¼ 17
18 72 6 1
13 59 4 3
22 101 12 1
7 7 1 2
(18) (74) (9) (1)
(16) (74) (5) (3)
(16) (74) (8) (0.7)
(41) (41) (5) (11)
Data represent the numbers of patients and numbers in parentheses are percentages. a Including overlapping cases: 2 patients in Group A þ B, 47 patients in Group A þ C, 18 patients in Group B þ C, 2 patients in Group B þ D, and 26 patients in Group A þ B þ C.
495
Table 7 Prevalence of pneumonia diagnosed by chest radiography or high-resolution computed tomography (HRCT) in 318 patients with suspected nursing and healthcare associated pneumonia. Pneumonia severitya
No. (%) diagnosed by chest radiography
No. (%) diagnosed by HRCT
p-Value
Mild Moderate Severe Very severe All patients
6 67 50 26 149
11 103 68 26 208
0.3257 0.0171 0.0826 >0.9999 <0.0001
(2) (21) (15) (8) (46)
(3) (32) (21) (8) (65)
a Pneumonia severity was classified by means of the A-DROP systems of the Japan Respiratory Society.
is still recommended as the standard reference method for confirming the diagnosis of pneumonia [1,13]. Some reports have indicated that CT images can more accurately provide detailed information about the lung parenchyma than a routine chest radiograph [16e18]. In this study, we found that pneumonia shadows were not detected by chest radiography in 59 (28.3%) out of 208 NHCAP patients. The detection failure rate of chest radiography was different among NHCAP criteria; 27.8% in Group A, 26.5% in Group B, 36.7% in Group C, and 5.8% in Group D. Chest radiography identified pneumonia cases at significantly lower rates than HRCT in Group A and Group C (Table 3). The most important difference between Groups A and C and Groups B and D was the frequency of poor functional status (PS grade 3 or 4) mainly owing to cerebrovascular disease. Thus, we believe that poor functional status may correlate with the low accuracy of chest radiography in diagnosing pneumonia. There have been some previous reports that assessed the diagnostic value of chest radiography for the identification of pneumonia in different types of respiratory tract infections. In a study of CAP, Syrjala et al. demonstrated that HRCT was superior to chest radiography for the identification of pneumonia (26 cases versus 18 cases; p ¼ 0.04) [16]. Pneumonia shadows were not detected by chest radiography in 8 (30.7%) out of 26 CAP patients. The same group also demonstrated that HRCT is more sensitive than radiography in detecting lower respiratory tract infectionrelated lung lesions in a primary care population [17]. Lower respiratory tract infection-related lung lesions were not detected by chest radiography in 8 (42.1%) out of 19 CAP patients. Although there were small numbers of patients in these study groups, the detection failure rate of chest radiography in CAP patients was higher than in our NHCAP study. To clarify the difference in CAP and NHCAP in terms of detection capability, a comparative study with CAP and NHCAP patients is needed. Chest CT studies in patients with aspiration pneumonia (classified as NHCAP and poor functional status) demonstrated that the lung opacities were distributed in the posterior lung fields and in the lower zone, and there was no anterior- or upper-predominant distribution [11]. In bedridden patients (classified as NHCAP and poor functional status), obtaining a lateral view is impossible, and the dome of the diaphragm may project over a significant portion of the lower zone. Thus, it may be difficult to interpret chest radiographs from patients with NHCAP, especially in patients with poor functional status [18]. Physicians should pay careful attention to the presence of pneumonia in patients with normal chest radiographic findings who have poor functional status. Diffuse aspiration panbronchiolitis (DAB) is a type of aspiration pneumonia that is characterized by chronic inflammation of bronchioles caused by recurrent aspiration of foreign particles in elderly patients [19,20]. Radiographically and pathologically at autopsy, DAB resembled diffuse panbronchiolitis [21]. The incidence of DAB in a total of 4880 autopsy cases was 0.64%, and 70% of
496
N. Miyashita et al. / J Infect Chemother 21 (2015) 492e496
patients with DAB were bedridden [19]. In our study, 18 (8%) of 208 NHCAP patients showed a radiographic pattern consistent with DAB. Thus, DAB is not a rare type among patients with NHCAP. There has been controversy regarding the benefit of chest CT for diagnostic purposes in general and because of the radiation risk in particular. However, Japanese physicians frequently use chest CT to assess patients suspected as having pneumonia, possibly because the healthcare insurance system in Japan allows clinicians to carry out CT. The benefit obtained with the use of HRCT may compensate for the higher cost in situations where a confident and prompt diagnosis is desirable. Further studies are needed to formulate costeffective recommendations. In conclusion, our results indicated that physicians often underestimate the pneumonia shadow in chest radiography in patients with NHCAP and the detection failure rate of chest radiography was different among NHCAP criteria. Poor functional status may correlate with the low accuracy of chest radiography in diagnosing pneumonia. Conflict of interest All of the authors have explicitly stated that there are no conflicts of interest in connection with this article. Acknowledgments This study was supported in part by MEXT KAKENHI (19591190 and 21591304) and Project Research Grants from Kawasaki Medical School (13-401, 14-402, 15-405A, 16-405M, 17-402M, 18-401, 19402M, 204030). References [1] Kohno S, Imamura Y, Shindo Y, Seki M, Ishida T, Teramoto S, et al. Clinical practice guidelines for nursing- and healthcare-associated pneumonia (NHCAP) [complete translation]. Respir Investig 2014;51:103e26. [2] Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 1982;5:649e55. [3] Miyashita N, Kawai Y, Akaike H, Yamaguchi T, Ouchi K, Hayashi T, et al. Clinical features and the role of atypical pathogens in nursing and healthcare-associated pneumonia (NHCAP): differences between teaching university hospital and community hospital. Intern Med 2012;51:585e94. [4] Ishida T, Tachibana H, Ito A, Yoshioka H, Arita M, Hashimoto T. Clinical characteristics of nursing and healthcare-associated pneumonia: a Japanese variant of healthcare-associated pneumonia. Intern Med 2012;51:2537e44.
[5] Fukuyama H, Yamashiro S, Tamaki H, Kishaba T. A prospective comparison of nursing- and healthcare-associated pneumonia (NHCAP) with communityacquired pneumonia (CAP). J Infect Chemother 2013;19:719e26. [6] Oshitani Y, Nagai H, Matsui H, Aoshima M. Reevaluation of the Japanese guideline for healthcare-associated pneumonia in a medium-size community hospital in Japan. J Infect Chemother 2013;19:579e87. [7] Kaku N, Yanagihara K, Morinaga Y, Izumikawa K, Nagashima S, Kakeya H, et al. The definition of healthcare-associated pneumonia (HCAP) is insufficient for the medical environment in Japan: a comparison of HCAP and nursing and healthcare-associated pneumonia (NHCAP). J Infect Chemother 2013;19: 70e6. [8] Nakagawa N, Saiato Y, Sasaki M, Tsuda Y, Mochizuki H, Takahashi H. Comparison of clinical profile in elderly patients with nursing and healthcareassociated pneumonia, and those with community-acquired pneumonia. Geriatr Gerontol Int 2014;14:362e71. [9] Teramoto S, Fukuchi Y, Sasaki H, Sato K, Sekizawa K, Matsuse T. High incidence of aspiration pneumonia in community and hospital acquired pneumonia in hospitalized patients: a multicenter, prospective study in Japan. J Am Geriatr Soc 2008;56:577e9. [10] Komiya K, Ishii H, Umeki K, Mizunoe S, Okada F, Johkoh T, et al. Impact of aspiration pneumonia in patients with community-acquired pneumonia and healthcare-associated pneumonia: a multicenter retrospective cohort study. Respirology 2013;18:514e21. [11] Komiya K, Ishii H, Umeki K, Kawamura T, Okada F, Okabe E, et al. Computed tomography findings of aspiration pneumonia in 53 patients. Geriatr Gerontol Int 2013;13:580e5. [12] The Committee for the Japanese Respiratory Society Guidelines in Management of Respiratory Infections. The Japanese Respiratory Society guideline for the management of hospital-acquired pneumonia in adults. Respirology 2008;14:S1e71. [13] The Committee for the Japanese Respiratory Society Guidelines in Management of Respiratory Infections. The Japanese Respiratory Society guideline for the management of community-acquired pneumonia in adults. Respirology 2006;11:S1e133. [14] Miyashita N, Kawai Y, Yamaguchi T, Ouchi K, Oka M, the Atypical Pathogen Study Group. Clinical potential of diagnostic methods for the rapid diagnosis of Mycoplasma pneumoniae pneumonia in adults. Eur J Clin Microbiol Infect Dis 2011;30:439e46. [15] Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159e74. [16] Syrjala H, Broas M, Suramo I, Ojala A, Lahde S. High-resolution computed tomography for the diagnosis of community-acquired pneumonia. Clin Infect Dis 1998;27:358e63. [17] Lahde S, Jartti A, Broas M, Koivisto M, Syrjala H. HRCT findings in the lungs of primary care patients with lower respiratory tract infection. Acta Radiol 2002;43:159e63. [18] Esayag Y, Nikitin I, Bar-Ziv J, Cytter R, Hadas-Halpern I, Zalut T, et al. Diagnostic value of chest radiographs in bedridden patients suspected of having pneumonia. Am J Med 2010;123. 88.e1e6. [19] Matsuse T, Oka T, Kida K, Fukuchi Y. Importance of diffuse aspiration bronchiolitis caused by chronic occult aspiration in the elderly. Chest 1996;110: 1289e93. [20] Matsuse T, Teramoto S, Matsui H, Ouchi Y, Fukuchi Y. Widespread occurrence of diffuse aspiration bronchitis in patients with dysphagia, irrespective of age. Chest 1998;114:350e1. [21] Homma H, Yamanaka A, Tanimoto S, Tamura M, Chijimatsu Y, Kira S, et al. Diffuse panbronchiolitis: a disease of the transitional zone of the lung. Chest 1983;83:63e9.