Incidental Findings on Whole-body Computed Tomography in Major Trauma Patients: Who and What?

Purpose Whole-body computed tomography (WBCT) scans are frequently used for trauma patients, and sometimes, nontraumatic findings are observed. We aimed to investigate the characteristics of patients with nontraumatic findings on WBCT. Methods From 2013 to 2016, adult trauma patients who underwent WBCT were enrolled. The proportions of nontraumatic findings in different anatomical regions were studied. Nontraumatic findings were classified and evaluated as clinically important findings and findings that needed no further follow-up or treatment. The characteristics of the patients with nontraumatic findings were analyzed and compared with those of patients without nontraumatic findings. Results Two hundred seventeen patients were enrolled in this study during the 3-year study period, and 89 (41.0%) patients had nontraumatic findings. Nontraumatic findings were found more frequently in the abdomen (69.2%) than in the head/neck (17.3%) and chest regions (13.5%). In total, 31.3% of the findings needed further follow-up or treatment. Patients with nontraumatic findings that needed further management were significantly older than those without nontraumatic findings (57.3 vs. 38.9; P < .001), particularly those with abdominal nontraumatic findings (57.9 vs. 41.3; P < .001). A significantly higher proportion of women were observed in the group with head/neck nontraumatic findings that needed further management than in the group without nontraumatic findings (56.3% vs 24.9%; P = .015). Conclusions Whole-body computed tomography could provide alternative benefits for nontraumatic findings. Whole-body computed tomography images should be read carefully for nontraumatic findings, particularly for elderly patients or the head/neck region of female patients. A comprehensive program for the follow-up of nontraumatic findings is needed.


Background
With the advent of spiral computed tomography and multislice scanning techniques, whole-body computed tomography (WBCT) scans have substantially increased over the last decades and have become a standard imaging modality to manage patients with major trauma because of its high diagnostic yield and wide availability. [1][2][3][4] A quick and complete overview of traumatic injuries in all relevant body regions (head to pelvis) can be performed using the technique.
In addition to traumatic findings, nontraumatic findings on WBCT scans are occasionally observed. These incidental findings might be beneficial to patients, such as earlier disease detection (eg, malignancy). However, they may also result in a high degree of patient anxiety and extra medical costs for a series of additional examinations; ultimately, the lesion might not affect the patient's health. Previous studies have reported that the rate of nontraumatic findings on WBCT in trauma patients ranges from 31% to 54% [5][6][7][8][9][10][11][12][13] and noted that those findings had poor follow-up rates (26.9%-48.4%). 5,6,9,10,14,15 Therefore, we aimed to investigate the proportion of nontraumatic findings on WBCT for major trauma patients at our institution. The characteristics of patients with nontraumatic findings on WBCT were evaluated. This information will help physicians improve care by modifying the interpretation of WBCT images and maintaining a higher index of suspicion for nontraumatic findings.

Methods
From June 2013 to May 2016, we retrospectively reviewed the Chang Gung Memorial Hospital (CGMH) trauma patient registry and medical records. CGMH is a level I trauma referral center with more than 3000 beds and serves more than 5 000 000 people in adjacent counties, and the emergency department (ED.) treats more than 25 000 trauma patients annually. At our institution, a 64-slice multidetector CT scanner is used to evaluate trauma patients. Additionally, the CT and resuscitation rooms are integrated in the same area of the ED. Patients with major trauma who had received WBCT were the focus of our study during this 36-month investigational period. 16 In the current study, patients with major trauma who received a WBCT examination were studied. Patients who were younger than 18 years, were too unstable to receive WBCT or had out-of-hospital cardiac arrest, failed to respond to resuscitation and subsequently died in the ED. without further treatment were excluded.
The WBCT protocol included an unenhanced scan of the head and neck, followed by a contrast-enhanced scan of the thorax, abdomen, and pelvis with a scanning range from the apex of the thoracic cage to approximately 5 cm below the symphysis. The contrast-enhanced scan was acquired after unenhanced head and neck computed tomography was performed. A bolus of iohexol (100 mL; Omnipaque 300 mg/mL) was administered as a continuous infusion at 3 mL/s. The thorax, abdomen, and pelvis were imaged after a delay of 70 seconds to acquire the postintravenous contrast images. The acquired axial images and routinely generated sagittal and coronal reconstructions were stored in and accessed using the picture archiving and communication system.
After the WBCT data were uploaded, the radiologic images were read by both a first-line trauma surgeon and a senior radiologist with expertise in trauma. The written radiologist interpretations of the WBCT examinations were reviewed for documented nontraumatic findings, which were defined as findings unrelated to the trauma. The investigator also checked the pictures and determined the presence of nontraumatic findings in the radiology report. If the nature of a finding (traumatic or nontraumatic) were not obvious on the image, the unblinded investigator would check the radiologic film and medical records during the ED. stay and hospitalization. The patient files, further imaging studies, and discharge diagnosis were reviewed to determine whether the finding was triggered by the current trauma. The medical charts during hospitalization and after discharge were also collected to evaluate the clinical consequences and follow-up outcomes.
Using the official report from the radiologist, the trauma surgeon or other physicians who managed the patients would decide the importance of the findings and categorize the nontraumatic findings into two groups according to clinical severity. 13 One group included findings that did not require intervention or further examination, and the other group included findings that were clinically significant and should be managed further (treatment or follow-up). Furthermore, patients with findings that were potentially severe and required immediate intervention were reported in detail separately.
In the present study, nominal data were presented as a percentage and were compared using Fisher's exact test, whereas numerical data were presented as means and standard deviation and were compared using independent samples t-test and one-way analysis of variance. All statistical analyses were performed using the SPSS software package (version 24.0). P < .05 was considered statistically significant.

Results
During the 36-month study period, 229 major trauma patients were admitted to our ED. with a WBCT scan. Twelve patients were excluded from the study for being younger than 18 years or having incomplete hospitalization documents or incomplete studies. Therefore, 217 patients with a mean age of 44.6 ± 18.4 years were enrolled in the study. Of these patients, 158 were men (72.8%) and 59 were women (27.2%). The mean injury severity score was 26.3 ± 12.3, and the mean hospitalization duration was 17.8 ± 14.7 days ( Table 1). The most common mechanisms of injury were traffic accidents (140/217, 64.5%) and falling down (58/217, 26.7%).
In the present study, 96.3% (209/217) of the patients had trauma-related findings, and 41% (89/217) had nontraumatic findings. The proportions of nontraumatic findings in the head/neck, chest, and abdomen were 10.6% (23/217), 7.8% (17/217), and 31.4% (66/217), respectively ( Table 2). Among the 89 patients with nontraumatic findings, 133 findings were recorded. The distribution of these nontraumatic findings is listed in Table 3 by an anatomic region. Diagnoses that were "clinically important and might need follow-up" or in "no need of follow-up" are shown. Of the diagnoses that were clinically important, thyroid nodules were the major nontraumatic findings of the head and neck (10/217, 4.6%). In the chest region, the major nontraumatic findings were lung nodules (6/217, 2.8%). In the abdominal region, spine spondylosis (14/217, 6.5%), gallbladder stones (13/217, 6.0%), and renal stones (7/217, 3.2%) were the top three nontraumatic findings that were clinically important. Table 4 shows the comparisons between patients with and without nontraumatic findings that needed further follow-up or treatment. Patients with nontraumatic findings that needed further management were significantly older than those without nontraumatic findings that needed further management (57.3 vs. 38.9; P < .001; whole body). When these nontraumatic findings were analyzed by different anatomical regions, age was not significantly different between these two groups in the head/neck or chest region subanalyses. However, patients with abdominal nontraumatic findings that needed further management were significantly older than those without abdominal nontraumatic findings that needed further management (57.9 vs. 41.3; P < .001). Furthermore, people aged 65 years or older were more likely to have nontraumatic findings that needed further management, both in the entire body and abdominal region. Similar comparisons were performed for sex between these groups. The group with head/neck nontraumatic findings that needed further management had a significantly higher proportion of female patients than that without head/neck abdominal nontraumatic findings that needed further management (56.3% vs. 24.9%; P = .015).
Six patients with severe findings required immediate evaluation and treatment (chronic type B aortic dissection, left intrahepatic duct intraductal papillary mucinous neoplasm, thyroid cancer, bilateral hydronephrosis, and porencephaly with midline shift of brain and left adrenal gland tumor); these data are shown in Table 5.
In the current study, five patients (2.3%) had incidental findings that were not mentioned in image reports during

Discussion
Whole-body computed tomography has been used frequently for major trauma patients worldwide. In addition to traumatic findings that require immediate management, Sierink et al reported an incidental finding rate of 44.5% (143/321) with traumatic WBCT in 2013. 5 Seah et al 6 also showed that 57/104 trauma patients (54.8%) had incidental findings identified on the WBCT radiologist report. Overall, the incidental finding rate in the previous literature ranged from 31% to 54%. [5][6][7][8][9][10][11][12][13] The results of the current study are consistent with those of previous studies (89/217, 41.0%). However, because of the critical condition of trauma patients who require WBCT, the images are usually read for traumatic findings. Thus, nontraumatic findings may be overlooked by first-line trauma surgeons or ED. physicians. Some of these nontraumatic findings could be life-threatening or require further evaluation and treatment. The nontraumatic findings on WBCT for trauma patients generally have poor follow-up rates (26.9% to 48.4%). 5,6,9,10,14,15 Although identifying and treating all WBCT findings are challenging, a comprehensive interpretation and follow-up plan are important for such nontraumatic findings. However, the distribution of nontraumatic findings was diverse among body regions and patients (Table 3). Some findings indicated an immediate need for treatment, some indicated close follow-up or continuous monitoring, some could not be identified by the primary imaging examination and needed further examinations, and some were harmless and did not indicate the need for any intervention. Patients might benefit from an early diagnosis of malignancies; however, these findings may increase anxiety and create extra medical costs for a series of additional examinations, and the lesion might not affect the patient's health ultimately. The fundamental and perhaps most important question is which patients have a higher probability of having nontraumatic findings that may indicate the need for early treatment?
Compared with patients without nontraumatic findings, those with nontraumatic findings were significantly older (57.3 vs. 38.9; P < .001). This aging effect is particularly important for findings in the abdomen (57.9 vs. 41.3; P < .001). In addition to several intra-abdominal malignancies, gallstone disease is one of the leading causes of digestion-related hospital admissions for elderly The findings in bold were considered clinically important and required further treatment or follow-up.
patients. 17,18 The frequency of gallstone disease varies among different countries and ethnic populations, as well as among various regions of each country. 19 In most developed countries, the overall prevalence of gallstone disease was reported to be between 10% and 20%. 20,21 Furthermore, previous studies have shown that the occurrence of gallstone disease increases with age, with a high prevalence rate at 50-60 years in both men and women. [21][22][23][24][25] Renal stones are also a common disease with a significant healthcare burden worldwide. Epidemiological studies show that the prevalence rate ranges between 4% and 20% in developed countries. 26,27 In Taiwan, the prevalence of upper urinary tract stones was reported to range from 2.85% to 9.6%. [28][29][30] Age is a risk factor for urolithiasis, particularly in individuals aged 50-60 years. [31][32][33][34] Nontraumatic findings are significantly more common in patients older than 40 years, as reported by previous studies. 10,14 As the average age of the modern population continues to increase and a corresponding increase in the average age of injured patients occurs, nontraumatic findings will become even more common and a greater patient care and medical-legal dilemma. Therefore, more attention should be given to the interpretation of WBCT images of elderly patients. Furthermore, an alert notification system for important incidental findings on WBCT may be needed. Even after admission, most physicians focus on a patient's traumatic findings and treat the major problems first. Some incidental findings noted on the WBCT performed before admission could be overlooked, causing patients to lose the clinical benefit. An alert notification of critical test results was reported to improve patient care. 35,36 The implementation of a similar system to interpret incidental findings on WBCT could be feasible and beneficial. Another point of interest is that female patients had more important nontraumatic findings in the head and neck than male patients (15.0% vs. 4.0%; P = .015). Among the 10 patients with thyroid nodules who were diagnosed incidentally with WBCT, 7 were women (11.9%) and only 3 were men (1.9%). Thyroid nodules are predominantly found in women. [37][38][39] Although most thyroid nodules are benign, thyroid cancer occurs in 4%-15% of patients with thyroid nodules. [40][41][42][43][44][45] The current guidelines suggest that individuals with thyroid nodules should receive follow-up care. 46 These findings suggest that WBCT images of the head and neck regions should be read carefully for women. Approximately 2.8% (6/217) of patients had nontraumatic findings that were potentially severe and needed further follow-up. Chronic aortic dissection (Stanford type B) was diagnosed incidentally with WBCT in a patient with a traumatic brain injury. After his trauma was treated, a thoracic endovascular aortic repair procedure was performed smoothly. One patient had abrupt tapering of the distal common bile duct and atrophy of the left liver on WBCT. This nontraumatic finding was recorded on the medical chart, and magnetic resonance imaging was performed accordingly by an outpatient department physician after discharge. Subsequently, an intraductal papillary mucinous neoplasm with biliary obstruction was diagnosed. Except for the above two patients, the other patients had no follow-up records of potentially severe incidental findings, even after discharge. ED physicians or trauma surgeons usually focus on patients' traumatic findings; thus, subacute lesions are overlooked.
Regarding the management of nontraumatic findings, a previous study has evaluated the use of midlevel providers to perform tertiary trauma surveys once the patients are admitted and notify those patients before discharge with appropriate follow-up plans. 15 Another study implemented a dedicated incidental finding coordinator for the detection and follow-up of nontraumatic findings, resulting in a more than 2.5-fold higher rate for identifying incidental findings and adequate follow-up both in the hospital and after discharge. 14 This approach represents a potential solution to this patient care and medical-legal dilemma in the future and will rely on collaborative efforts between radiologists, trauma and emergency physicians, and primary care physicians. Primary care physicians should value those nontraumatic findings more and arrange examinations, interventions, or outpatient department follow-up examinations when the patients are discharged from the ward. More immediately, however, frontline trauma staff must be vigilant about discussing the nontraumatic findings with their discharged patients to ensure that all the patients have appropriate follow-up care arranged.
Based on the results of the current study, our simple classification (need for treatment/follow-up or not) simplifies the grading process for first-line ED physicians or trauma surgeons by recording whether treatment/followup is needed. This classification allows physicians to spend less time shifting the patient to the ward, without losing important incidental findings recorded in the medical chart. Further management (treatment or followup) could be decided by subspecialists after admission. Furthermore, a standard protocol for image interpretation has been established for radiologists. Both traumatic and nontraumatic findings could be recorded systemically. An alert notification (short message service or email) would then be sent to physicians managing the patient currently by the radiologist when important findings (both traumatic and nontraumatic findings) are identified on WBCT. Additionally, the first-line ED physicians or trauma surgeons record the findings and emphasize those needing follow-up in the medical chart record. They are also requested to shift delivery of the patient to the physicians in charge of that ward by person-to-person communication.
Before patients are discharged, the outpatient department schedules appointments to specialists if needed. Otherwise, trauma case managers will contact patients after discharge and remind them if a finding needed follow-up. The limitations of this study include its retrospective nature and limited patient sample from a single institution. Although we manage many trauma patients in our ED. per year, only a small proportion of patients with WBCT were enrolled in the current study. This skewed proportion may be due to a debate between the pan scan and specified CT scan. Additionally, the regulation of medical expenditure by the national insurance system in Taiwan also contributes to this effect. Thus, possible selection bias may have limited our conclusions. The WBCT protocol was designed for trauma patients. Therefore, the images of the head and neck were non-contrast enhanced. Under this condition, some lesions that need contrast enhancement for diagnosis could not be detected. Additionally, the general use of WBCT for all trauma patients is infeasible because of the biohazards of radiation exposure and expanded medical cost. Another concern is that some findings were difficult to define, making it challenging to determine whether they should be included in this study. For example, spinal degenerative changes were only reported in severe cases that could be observed on imaging. A reporting threshold might be needed for minor cases. Further, studies with larger sample sizes and prospective designs are needed to establish an accurate interpretation system to comprehensively evaluate both traumatic and nontraumatic findings.

Conclusions
Whole-body computed tomography could provide alternative benefits for nontraumatic findings. WBCT images should be read carefully for nontraumatic findings, particularly for elderly patients. For female patients, the head/ neck region of the WBCT scan should be evaluated carefully for possible thyroid lesions. A comprehensive program for the follow-up of nontraumatic findings is needed.
Analysis and interpretation of the data: Ping-Yuan Liu and Chih-Yuan Fu. Drafting of the manuscript: Ping-Yuan Liu. Critical revision: Ling-Wei Kuo and Francesco Bajani.

Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval
This retrospective study was approved by the Institutional Review Board of Chang Gung Memorial Hospital.