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Risk factors for detection failures of chest radiography in diagnosing pneumonia

Abstract Background Little is known about clinical factors associated with undetectable pneumonic shadows on chest radiographs (CRs) for diagnosing pneumonia in the primary care setting. Methods A retrospective assessment of CRs was conducted to compare chest computed tomography (CT) images of patients admitted to Kesennuma City Motoyoshi Municipal Hospital who were diagnosed with pneumonia from April 2014 to June 2016. Results Eighty‐three patients were included, and their average age was 83.8 years. Sixty‐eight patients (81.9%) were officially certified as requiring long‐term care or support. Twenty‐nine of the 83 patients (34.9%) had either negative or normal findings on CRs, and positive findings consistent with pneumonia on CT. There were no significant differences in gender, age, cardiothoracic ratio on CR, or severity between the CR‐negative and CR‐positive groups. The proportion of negative CRs was significantly higher in patients with certified care level 5 under the long‐term care system in Japan and tube feeding. Conclusion The failure rate of CRs for detecting pneumonic shadows was significantly higher in patients with certified care level 5 and tube feeding.


| INTRODUCTION
Radiographic examination has an important role in the diagnosis and evaluation of pneumonia. According to Infectious Diseases Society of America/American Thoracic Society Consensus Guidelines on the management of community-acquired pneumonia, a demonstrable infiltrate by chest radiograph (CR) or other imaging technique is required for the diagnosis of pneumonia in addition to a constellation of suggestive clinical features. 1 Although computed tomography (CT) is much more sensitive than chest radiography and can detect pneumonic shadows, which are difficult to identify on CRs, the greater cost and higher radiation exposure limit its use as a screening modality. There is little evidence to support the role of CT in diagnosing pneumonia.
Japanese guidelines on imaging diagnosis for community-acquired pneumonia (CAP) have given a grade C recommendation (lacking direct evidence) for the use of CT only in situations where CRs are negative for the presence of pneumonia despite a strong clinical suspicion. 2 According to the British Thoracic Society guidelines for the management of CAP, CT currently has no routine role in the investigation of CAP. 3 There are several studies that reported the superiority of CT to chest radiography for detecting pneumonia. [4][5][6][7][8][9] Although CT is more sensitive in diagnosing pneumonia and may be more specific for certain pathogens than chest radiography, objective guidelines regarding its indication are lacking. 10 Furthermore, whether CT improves the prognosis of pneumonia patients has not been revealed.
This study aimed to identify risk factors for undetectable pneumonic shadows on CRs compared to CT, and to clarify whether certain patients benefit from CT for diagnosing pneumonia.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

| Baseline characteristics
During the study period, we enrolled and analyzed 83 patients. The reasons for performing CT were to confirm the diagnosis, evaluate severity, discriminate from noninfectious diseases, or presume causal pathogens. All patients' characteristics are summarized in Table 1.

| Radiographic findings
Twenty-nine of the 83 patients (34.9%) had either normal or negative findings on CRs, and positive findings consistent with pneumonia on CT images.
The reasons negative findings were noted on CRs were as follows (numbers include overlapping cases): 1. The pneumonic shadows were dominantly distributed over basilar lung fields, and the dome of diaphragm projected on the shadows (18 cases).

2.
The pneumonic shadows were too tiny or too light (17 cases).

3.
Anatomic structures, such as the heart, vessels, and bones, superimposed to impair the pneumonic shadows (six cases). The characteristics of patients according to the radiographic findings are summarized in Table 2. For detecting pneumonic shadows, chest radiography was significantly inferior to CT for patients with certified care level 5 and tube feeding. Conversely, there were no significant differences between the two groups for gender, age, resident status, CTR, and severity.

| Subgroup analysis
We performed subgroup analysis among patients with certified care level 5 to clarify the clinical characteristics of the worst PS patients (n=21). Mortality was significantly lower in the CR-negative group, while there were no significant differences between the two groups in severity and other factors (Table 3).

| DISCUSSION
Pneumonia is the third most frequent cause of death in Japan.
Approximately 97% of pneumonia patients are 65 years or older. The proportion of individuals 65 years or older among the total population in the Kesennuma Motoyoshi area, where our hospital is located, was 33.8% in 2015. Population aging has been progressive in our area.
In this study, 91.6% were 65 years or older, the average age of the patients was as high as 83.8 years, and more than 80% of them were officially certified as requiring long-term care or support.
Conventionally, pneumonia is classified as CAP and hospitalacquired pneumonia. In 2011, the JRS documented a new pneumonia category termed nursing-and healthcare-associated pneumonia (NHCAP). 11 This category is distinct from CAP and is relevant to the Japanese population, the Japanese healthcare insurance system, including the nursing-care insurance system, and for the pattern of drugresistant pathogens. The criteria for NHCAP are as follows: distribute to the lower and dorsal zone of the lung, 13,14 chest radiography might be unable to detect the shadow due to the dome of the diaphragm projecting over a significant portion of the lower zone of the lung. In our study, 18 of 29 patients (62.1%) showed negative findings on CRs because the pneumonic shadows were dominantly distributed over basilar lung fields. Although lateral CRs might be useful for detecting the shadows, it was difficult to take lateral views for the poor PS patients. In addition, most of the poor PS patients could undergo chest radiography in the prone or sitting position only, and they could not obey the instruction of inspiration. As a result, the diaphragm would be in a relatively higher position in CRs and cover the pneumonic shadows.
In this study, tube feeding was also the significant risk factor for negative CR findings. There is no evidence that tube feeding reduces the risk of the aspiration pneumonia. 15,16 Conversely, tube feeding is a risk factor for aspiration pneumonia because of reflux and chronic occult aspiration. It is presumable that most of the tube feeding patients' pneumonia was caused by aspiration, and CRs noted negative findings for the reasons mentioned above.
There are a few studies that reported the usefulness of CT for the early diagnosis of pneumonia, although patients' prognoses have not been reported. With regard to severe acute respiratory syndrome (SARS)-associated coronavirus pneumonia, there was a study reported that CT was useful for the early diagnosis of pneumonia in patients with normal CRs. 17 For pneumonia in febrile neutropenic patients, there was a report that CT could detect pneumonic shadows approximately 5 days earlier than CR. 9 Our subgroup analysis performed among care level 5 patients showed significantly lower mortality in the CR-negative group irrespective of severity. Although it would be difficult to clarify the relationship between radiographic findings and prognosis using the retrospective survey seen in the current study, we think that CT contributes to early diagnosis, early treatment, and better prognosis for pneumonia patients with poor PS and negative CR findings. Additionally, our data showed that 31.0% of the CR-negative group had an A-DROP score of 3 or more. It was notable that CRs sometimes could not show positive findings even though pneumonia was severe.
This study had several limitations. We did not include all patients with pneumonia admitted to our hospital, and there may have been a selection bias through including only the patients who underwent chest radiography and CT on the same day. Even performed on the same day, the time lag between the chest radiography and CT may have influenced the outcome because it is conceivable that the chest radiography findings changed from negative to positive during the few hours before the CT scan was performed. A further limitation is related to radiological diagnosis ability; only part of the chest CT image was surveyed by a radiologist from another facility, and no radiologists participated in the interpretation of the CRs. To accurately evaluate the radiographic findings, all CT images and CRs should be surveyed by two or more radiologists, and the Cohen's kappa coefficient should be calculated to measure interobserver agreement regarding the interpretation of the images. However, this was logistically difficult at our hospital.
The population has progressively been aging in Japan, and pneumonia patients who need care at a high level or with tube feeding will increase. It should be taken into consideration that some patients do not show positive chest radiography findings even with severe pneumonia. CT may be useful and may contribute to the early diagnosis and treatment of patients with equivocal clinical findings and negative CRs.