ORIGINAL ARTICLE Ultrasound Evaluation of Skull Fractures in Children A Feasibility Study Antonio Riera, MD and Lei Chen, MD Objective: The objective of this study was to investigate feasibility and evaluate test characteristics of bedside ultrasound for the detection of skull fractures in children with closed head injury (CHI). Methods: This was a prospective, observational study conducted in a pediatric emergency department of an urban tertiary care children s hospital. A convenience sample of children younger than 18 years were enrolled if they presented with an acute CHI, and a computed tomography (CT) scan was performed. Ultrasound was performed by pediatric emergency medicine physicians with at least 1 month of training in bedside ultrasound. Ultrasound interpretation as either positive or negative for the presence of skull fracture was compared with attending radiologist CT scan dictation. Test characteristics (sensitivity, specificity, and positive and negative predictive values) were calculated. Results: Forty-six patients were enrolled. The median age was 2 years (range, 2 months to 17 years). Eleven patients (24%) were diagnosed with skull fractures on CT scan. Bedside ultrasound had a sensitivity of 82% (95% confidence interval [CI], 48%Y97%), specificity of 94% (95% CI, 79%Y99%), positive predictive value of 82% (95% CI, 48%Y97%), and negative predictive value of 94% (95% CI, 79%Y99%). Conclusions: Bedside ultrasonography can be used by pediatric emergency medicine physicians to detect skull fractures in children with acute CHI. Larger studies are needed to validate these findings. Future studies should investigate the role of this modality as an adjunct to clinical decision rules to reduce unnecessary CT scans in the evaluation of acute CHI in children. Key Words: ultrasound, head injuries, fractures, computed tomography (Pediatr Emer Care 2012;28: 420Y425) Pediatric closed head injury (CHI) is a common condition in the emergency department. Of the 600,000 children who are seen annually for blunt head trauma in the United States, roughly 15% will have some type of intracranial injury. 1 Skull fractures are the most common abnormal findings encountered after CHI. Computed tomography (CT) scan of the brain is the diagnostic test of choice to evaluate for skull fractures and intracranial injuries. 2 The presence of a skull fracture is strongly associated with underlying intracranial injury, with 1 study finding a 4- fold increase in the relative risk of intracranial injury. 3 In general, skull radiography adds little benefit to the evaluation of From Yale University School of Medicine, New Haven, CT. Disclosure: The authors declare no conflict of interest. Reprints: Antonio Riera, MD, Yale University School of Medicine, 100 York St, Suite 1F, New Haven, CT 06511 (e-mail: Antonio.riera@yale.edu). This study was supported in part by CTSA, grant KL2 RR024138 from the National Center for Research Resources, a component of the National Institutes of Health (NIH), and NIH Roadmap for Medical Research. Abstract platform presentation: Eastern Society of Pediatric Research, March 2010, Philadelphia, PA. Poster presentation: Pediatric Academic Society, May 2010, Vancouver, British Columbia, Canada. Copyright * 2012 by Lippincott Williams & Wilkins ISSN: 0749-5161 patients who are at high risk for intracranial injury. 4Y6 Although skull radiography can be used to detect skull fractures, the sensitivity and specificity for the detection of skull fractures are not clearly established. Children younger than 2 years with nonfrontal scalp hematomas have increased risks for skull fractures and intracranial injuries. 4,7 It is unclear whether this particular subset of patients, who may be otherwise well appearing, truly benefits from some kind of screening evaluation for skull fractures before head CT scanning. The decision to perform a CT scan is a complex one, especially for infants and toddlers. This is due to physiologic and behavioral differences of younger children. History is often not reliable. Children may be asymptomatic at the time of evaluation. Children can be alert at the time of initial evaluation, without clinical signs of brain injury except the presence of a scalp hematoma. One prospective study showed that 1 in 14 asymptomatic infants younger than 2 years with CHI required surgical intervention. 8 Some advocate that any child younger than 3 months with a nontrivial injury should receive a head CT, because of the high incidence of intracranial injury in this subgroup with a normal initial physical examination. 4 The cumulative risks from ionizing radiation of CT scans are present, yet difficult to quantify. Specifically, expert panel consensus states that it is reasonable to assume that the low-level radiation used in diagnostic imaging may have a small incremental risk of causing cancer. 9 The risks are likely higher for younger children, precisely the group in which history and physical examination data are less reliable. 10 Multiple studies have been conducted to derive clinical prediction rules to identify patients at low risk for traumatic brain injury, thereby obviating the need for a head CT. In general, these decision pathways yield high sensitivity scores (98%Y99%) at the expense of lower specificity. 7,11,12 Studies have shown poor interobserver agreement with parameters such as severe headache and abnormal mental status during the application of these rules. 13 A large number of CT scans are still performed in children after blunt head trauma, with the vast majority of them revealing no abnormalities. Emergency department physicians must weigh the benefits of early diagnosis of intracranial pathology with the increased cost associated with a CT scan, the child s exposure to radiation, and the potential adverse effects of sedative medications. Ultrasound is an imaging modality that could be used to evaluate for the presence of skull fractures, which are strongly associated with intracranial injuries. There is good evidence to support the use of bedside ultrasonography to detect long-bone skeletal fractures. 14,15 A limited number of studies have assessed the potential role of ultrasound in the setting of head trauma. 16Y18 These articles either used transfontanellar imaging to assess for intracranial injury or had incomplete comparison testing of skull ultrasounds. Two recent articles have described the ability of point-of-care ultrasound to detect skull fractures in a small number of patients. 19,20 However, no research to date has rigorously and specifically compared ultrasound to CT for the detection of skull fractures in children. 420 www.pec-online.com Pediatric Emergency Care & Volume 28, Number 5, May 2012
Pediatric Emergency Care & Volume 28, Number 5, May 2012 Ultrasound Evaluation of Skull Fractures TABLE 1. Demographics Study Population n = 46 Median age (range) 2 y (2 mo to 17 y) Age G2 y, n (%) 19 (41) Age 92 y, n (%) 27 (59) Sex, n (%) Male 31 (67) Female 15 (33) Hematoma/impact site, n (%) Frontal 16 (35) Parietal 15 (33) Occipital 9 (19) Temporal 4 (9) Periorbital 2 (4) Goal of Study The goal of this pilot study was to investigate the test characteristics of ultrasound in the diagnosis of skull fractures in children after acute CHI. The preliminary data could help guide the design and execution of a larger multicenter trial. In addition, we hoped to identify relevant scanning techniques and potential pitfalls of bedside skull ultrasonography. METHODS Study Design and Setting This was a prospective study of pediatric emergency department (PED) patients who underwent CT scan as part of their evaluation for CHI. The study was performed in an urban PED of a tertiary care, level I trauma, children s hospital from February 2009 to July 2010. The PED has an annual census of approximately 32,000 visits per year. Bedside skull ultrasonography was performed by pediatric emergency medicine physicians and compared with the attending radiologist dictation of corresponding CT scans. Radiologists were not aware of ultrasound findings at the time of their dictation. Sonographers were occasionally aware of the CT findings at the time bedside sonography was performed. The study was approved by our institutional human investigation committee, and informed consent and assent were obtained from subjects and their parents. TABLE 2. Bedside Ultrasound Compared With CT for the Detection of Skull Fractures: All Studies CT + CT j BUS + 9 2 BUS j 2 33 BUS indicates bedside ultrasound. TABLE 3. Bedside Ultrasound Compared With CT for the Detection of Skull Fractures: Prospective Studies CT + CT j BUS + 3 2 BUS j 2 33 BUS indicates bedside ultrasound. Subject Enrollment Children aged 0 to 18 years with acute CHI were eligible for the study. A convenience sample of subjects was enrolled based on the availability of participating sonographers. Subjects were eligible for enrollment if they underwent a CT scan of the head as part of their evaluation and had either a scalp hematoma or some other localizable point of impact on physical examination. Subjects were excluded if they presented with open fractures, a suspicion for nonaccidental trauma, or if urgent intervention (ie, intubation or expeditious neurosurgical treatment) was required. Methods Related to Sonography Bedside ultrasounds were performed by 4 pediatric emergency medicine physicians (2 attending physicians and 2 fellows). One sonographer (L.C.) had 10 years of clinical and research experience with pediatric emergency ultrasound. The other participating sonographers had 1 month of dedicated ultrasound exposure and training through a clinical rotation in our institution s adult emergency department. Consultation with the chief of Pediatric Radiology was obtained to confirm study viability. Ultrasonography was performed using the L38 linear transducer (5Y10 MHz) of a SonoSite MicroMaxx ultrasound system (SonoSite, Bothell, Wash). After the application of ultrasound gel or use of either a stand-off pad or water-filled glove, the transducer was placed over the area of soft tissue swelling or point of impact. Images were scanned in 2 orthogonal planes throughout the length of the hematoma, when present. For quality assurance, images were saved and made available for further review. The sonographers recorded a real-time interpretation of the ultrasound as either positive or negative for a skull fracture (depicted by either an intact hyperechoic bony cortex or a visible break in the bony cortex). The sensitivity, specificity, positive predictive value, and negative predictive were determined using the CT scan dictation as the comparison standard. No previous data exist to guide the sample size calculation for this exploratory pilot study. RESULTS Patient characteristics are listed in Table 1. Forty-eight total patients and their families were approached for enrollment. One potential subject was not enrolled because parents did not wish to participate in the study (they were already aware of their son s CT scan results). Another potential subject was TABLE 4. Test Characteristics of Bedside Ultrasound for the Detection of Skull Fractures All Studies (95% Confidence Interval) Prospective Studies (95% Confidence Interval) n 46 40 Sensitivity, % 82 (48Y98) 60 (17Y93) Specificity, % 94 (79Y99) 94 (79Y99) PPV, % 82 (79Y99) 60 (17Y93) NPV, % 94 (48Y98) 94 (79Y99) PPV indicates positive predictive value; NPV, negative predictive value. * 2012 Lippincott Williams & Wilkins www.pec-online.com 421
Riera and Chen Pediatric Emergency Care & Volume 28, Number 5, May 2012 FIGURE 1. A, Comminuted occipital skull fracture in a 2-month-old child as seen on bedside ultrasound. B, Comminuted occipital skull fracture in a 2-month-old child as seen on corresponding CT scan. excluded after bedside ultrasound was obtained because the parents refused the CT scan. No subjects were excluded because they required urgent intervention. A total of 46 subjects were included in the analysis. Four physicians enrolled patients. Study physician 1 (A.R.) enrolled 27 patients. Study physician 2 (L.C.) enrolled 16 patients. Study physicians 3 and 4 combined to enroll the remaining 3 patients. Good patient cooperation was observed throughout except with subject 10 (a 1-year-old boy who did not tolerate placement of the ultrasound probe on his head). This child went on to have a limited, nondiagnostic ultrasound (interpreted as no visible fracture for the purposes of this research) with a positive CT scan. The incidence of skull fractures on CT scan was 24%. The incidence of intracranial bleeding was 6.5%. A skull fracture was present in 2 of the 3 cases with intracranial bleeding. Table 2 represents the results of bedside ultrasound compared with official CT scan reports for all subjects enrolled. Table 3 represents the results of bedside ultrasound compared with official CT scan reports for prospective ultrasounds done at our institution. The majority (87%) of bedside ultrasounds were performed prospectively. There were 3 cases in which the ultrasound was performed after CT results were known and 3 cases in which a patient was transferred from a referring hospital with CT imaging already done. Test characteristics of bedside ultrasonography comparing all studies and prospective studies are listed in Table 4. Two cases are included to show skull fractures as diagnosed on ultrasound with their corresponding CT scan images (Figs. 1A, B; Figs. 2A, B). DISCUSSION We have demonstrated that ultrasound can be used to detect skull fractures in children after CHI. This finding corroborates with prior research, which has shown ultrasound as a viable alternative to radiography in the detection of long-bone and clavicle fractures. 14,21,22 In addition, we found high specificity but lower sensitivity for the detection of skull fractures using bedside ultrasound. The high specificity that was observed is similar to other diagnostic ultrasound indications in emergency settings for children, such as the diagnosis of acute appendicitis. 23 Although ultrasound specificity remained excellent at 94% the positive predictive value of prospectively enrolled subjects, a subgroup with a significantly lower prevalence of skull fractures, decreased to 60%. Careful attention should be paid to these different rates of skull fractures when comparing the overall test characteristics results to the prospective findings. There are several potential advantages of ultrasound for the detection of skull fractures. Bedside ultrasound can usually be performed quicker than obtaining a CT scan. Earlier detection of skull pathology would lead to earlier consultation of neurosurgical services and help prioritize follow-up CT scan. This is important because in many cases of intracranial injury, FIGURE 2. A, Linear temporal skull fracture in an 11-year-old child as seen on bedside ultrasound. B, Linear temporal skull fracture in an 11-year-old child as seen on corresponding CT scan. 422 www.pec-online.com * 2012 Lippincott Williams & Wilkins
Pediatric Emergency Care & Volume 28, Number 5, May 2012 Ultrasound Evaluation of Skull Fractures FIGURE 3. Nondisplaced linear skull fracture and parietal scalp hematoma in a 1-year-old child. Note that the fracture line lies adjacent to the hematoma. rapid diagnosis and management lead to improved outcomes. More importantly, if used appropriately, it can further reduce head CT imaging in young patients after CHI. The diagnostic conundrum for emergency physicians is that the youngest patients with intracranial injury are often asymptomatic early in the course of their injury, yet are also the most sensitive to the effects of ionizing radiation by CT scan. 10 Studies have shown that in children younger than 2 years with a linear skull fracture, the incidence of intracranial injury is 15% to 30%. The incidence of skull fractures among children with intracranial injury ranges from 60% to 100%. For children with minor head trauma, skull fractures are a better predictor for intracranial injury than clinical symptoms. 4 Incorporation of bedside ultrasound into clinical decision rules could further risk stratify these patients and reduce exposure to the potentially harmful effects of radiation. There also exists the possibility that ultrasound may help identify cases of skull fractures that are missed on CT scan. The literature on pediatric facture diagnosis using ultrasound suggests that, in certain type of fractures, ultrasound has greater sensitivity when compared with radiography. 24 The following case from our sample illustrates this point. A 6-month-old female infant presented to our PED after a fall from a booster chair at home from a height of about 4 ft. She initially looked well. A bedside ultrasound detected a parietal skull fracture. Her CT scan was read as negative for intracranial abnormality or skull fracture. She was discharged home. Shortly after arriving home, she developed multiple episodes of vomiting and became lethargic. She was brought back to the ED where a second head CT was performed, which revealed the nondisplaced parietal skull fracture with no intracranial bleeding. She was admitted for supportive care. An addendum was made to the initial CT scan where a parietal skull fracture was retrospectively noted. We included this case in the ultrasound-positive and CT-negative group to reflect the initial dictation of the first CT scan by an attending radiologist. Interpretation of this case as a true positive ultrasound for the detection of skull fracture would have changed this study s overall test characteristics to a sensitivity of 83%, specificity of 97%, positive predictive value of 91%, and negative predictive value of 94%. A potential pitfall is that a linear skull fracture may be missed because it lies adjacent to the hematoma and not directly underneath. This pattern of injury has been reported in the literature for nonaccidental trauma. A blunt impact to the cranium will cause the underlying skull to bend inward at the point of impact and a more peripheral area of the skull to bend outward. It is at the region of outward bending that a linear skull fracture begins, with potential extension toward the impact site during the rebound phase of trauma. 25 That said, review of all CT-positive skull fractures with overlying hematomas in this case series revealed that only 1 (10%) case of 10 displayed a fracture line visible adjacent and not directly underneath the scalp hematoma (Fig. 3). This occurred in study subject 10 who was the lone subject who did not fully cooperate with ultrasound examination. It is possible that, using dynamic oblique imaging through the entire hematoma, the fracture line would have been observed in a more cooperative patient. The use of a peripheral stand-off pad or water filled glove is another option that may increase sensitivity. Future studies should take this into consideration to better investigate this phenomenon. Another issue which we encountered is how to best image the cranium when hair impedes the use of ultrasound gel. In general, either the use of a water filled glove or a stand-off pad can provide adequate images to interpret the presence or absence of a skull fracture. When using a water-filled glove, a mirror image artifact is created, because the skull bones are curved structures that strongly reflect ultrasound. In addition, reverberation caused by repeated reflections of an object near the transducer may create numerous horizontal lines posteriorly (Fig. 4A). FIGURE 4. A, Ultrasound imaging of the skull using a water-filled glove. Note the many floating white particles in the most superficial hypoechoic space, which depict motion of water. The most superficial hyperechoic line represents an intact skull bone without evidence of fracture. Mirror image and reverberation artifacts are seen. B, In this image, the probe is directly over a hematoma, and mirror imaging is again observed. Note that an intact skull line is represented by the most superficial hyperechoic stripe on the screen. Interpretation of the reverberation artifact depicted by the deeper hyperechoic lines as a fracture should be avoided. * 2012 Lippincott Williams & Wilkins www.pec-online.com 423
Riera and Chen Pediatric Emergency Care & Volume 28, Number 5, May 2012 FIGURE 5. A, Metopic suture observed on ultrasound and CT in a 4-month-old child with a small frontal scalp hematoma. Note the symmetric alignment of separated bone and relatively narrow separation. B, Metopic suture in a 4-month-old child as seen on corresponding CT scan. Mirror imaging of scalp hematomas may also be observed when one does not use a water-filled glove or stand-off pad (Fig. 4B). Knowledge of suture line anatomy is another important component for the sonographic evaluation of newborn and infant skulls. It may be difficult to distinguish if the separation of bone underneath a hematoma is due to a nondisplaced linear fracture or simply a normal suture line. Several techniques can be used to perform a best estimate. First, if the separation looks irregular, jagged, or not properly aligned (as opposed to a symmetric alignment of separated bone), it is more suggestive of a fracture. Second, evaluation and comparison to a contralateral suture, when present, can be helpful. The images in Figure 5A and B represent a normal suture line underneath a frontal hematoma in a 4-month-old child. Currently, no standardized sonographic measurements exist of suture anatomy, which can serve as an area for future study. Limitations Our study has several limitations. First, 6 ultrasounds (13%) were obtained with knowledge that a skull fracture was present on CT scan and/or that a patient was referred for a higher level of care after a CT scan was done at an outlying hospital. The majority of these cases were performed in the early stages of data collection. Although not ideal for research purposes, we felt it was important to capture these patients and report the bedside ultrasound findings. We hoped to evaluate a sufficient number of positive ultrasounds to make meaningful conclusions about bedside ultrasound s ability to detect skull fractures. Because only a select group of emergency physicians was eligible to enroll patients, there was a possibility that not enough subjects with skull fractures would be enrolled. We acknowledge that bias introduced by unblinded ultrasounds limits the overall test characteristic findings of this feasibility study. A total of 4 physicians enrolled patients and performed bedside ultrasounds. Image acquisition and interpretation of diagnostic ultrasound are operator-dependent. The sonographer s experience, hand-eye coordination, manual dexterity, and overall comfort with the machine all influence the ability to effectively use ultrasound as a diagnostic tool. We recognize that different levels of skill and experience existed between our study sonographers. We did not offer a standardized didactic session, nor did we perform practice musculoskeletal ultrasounds to evaluate different types of fractures. We did not measure for rates of interoperator agreement. Future studies addressing these issues should be performed. CONCLUSIONS Bedside ultrasonography can be used by pediatric emergency medicine physicians to detect skull fractures in children with acute CHI. Larger studies are needed to validate these findings. Future studies should investigate the role of this modality as an adjunct to clinical decision rules to reduce unnecessary CT scans in the evaluation of acute CHI in children. ACKNOWLEDGMENTS The authors thank Rob Goodman, MD (associate professor of diagnostic radiology and chief of Pediatric Imaging at YaleY New Haven Children s Hospital), for his guidance and support with this project. The authors also thank Melissa Langhan, MD, and Amy Doolan Roy, MD, for their participation with subject enrollment. REFERENCES 1. Division of Injury Control, Center for Environmental Health and Injury Control, Centers for Disease Control. Childhood injuries in the United States. Am J Dis Child. 1990;144:627Y646. 2. 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