CLINICAL STUDY
Incidental Findings on Preoperative Computed Tomography for Nonsyndromic Single Suture Craniosynostosis Keshav T. Magge, MD, Suresh N. Magge, MD, Robert F. Keating, MD, John S. Myseros, MD, Michael J. Boyajian, MD, Tina M. Sauerhammer, MD, Gary F. Rogers, MD, JD, and Albert K. Oh, MD Abstract: Although the diagnosis of nonsyndromic single suture craniosynostosis (NSSC) can usually be made by clinical examination, computed tomography (CT) is still commonly used in preoperative evaluation. This practice has been questioned in light of recent studies that document a small, but measurable, increased risk of malignancy from CT-associated radiation. The purpose of this study was to examine whether preoperative CT for patients with NSSC provided clinically important information beyond confirmation of craniosynostosis. We performed a retrospective analysis of all patients with NSSC undergoing cranial vault remodeling at our center from March 1999 to March 2011. Only patients with complete preoperative CT scans available for review were included. Staff pediatric neurosurgeons were blinded to patient diagnosis and official radiology report, analyzed the CT images, and documented the site of synostosis and any other findings. Of the 231 patients, 80 met the inclusion criteria. Sites of synostosis included sagittal (51 patients), coronal (17 patients), metopic (11 patients), and frontosphenoidal (1 patient). Clinical diagnosis correlated with radiographic site of fusion in all patients except the patient with frontosphenoidal synostosis. Incidental findings were documented in more than 50% of the patients including prominent extra-axial cerebrospinal fluid (n = 36, 45%), ventriculomegaly (n = 5, 6.25%), choroid fissure cyst (n = 2), cavum septum pellucidum (n = 2), Chiari malformation (n = 1), and prominent perivascular space (clinically nonsignificant finding, n = 1). Incidental findings required additional follow-up or management in 5 patients (6.25%). Our findings support the use of preoperative imaging in this population to identify intracranial anomalies that cannot be discerned
From the Division of Plastic and Reconstructive Surgery and the Division of Neurosurgery, Children's National Medical Center, George Washington University. Received December 17, 2013. Accepted for publication January 17, 2014. Address correspondence and reprint requests to Albert K. Oh, MD, Children's National Medical Center, 111 Michigan Ave, NW, Washington, DC 20010; E-mail: [email protected] Presented in part at the 12th International Congress on Cleft Lip/Palate and Related Craniofacial Anomalies, May 2013, and at the International Society of Craniofacial Surgery, 15th Biennial Meeting, September 2013. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000797
by clinical examination. Whereas many findings were not clinically important, some required additional attention. Key Words: Preoperative evaluation, craniosynostosis, incidental radiologic findings (J Craniofac Surg 2014;25: 1327–1330)
M
ore than 150 years ago, Virchow proposed that fusion of cranial sutures produced predictable changes in cranial shape.1 The natural corollary of this hypothesis is that most forms of single suture craniosynostosis can be diagnosed by clinical examination. This tenet is nearly universally accepted, yet confirmatory computed tomography (CT) scan is still the standard practice in most centers. Opponents of routine diagnostic CT evaluation for nonsyndromic single suture craniosynostosis (NSSC) suggest that the test is rarely required to make the diagnosis, adds to the cost of delivering care, and occasionally requires general anesthesia.2 Their argument is further reinforced by a series of recent reports highlighting the deleterious effects of ionizing radiation on infants. Brenner and Hall3 showed that the estimated lifetime cancer mortality risks attributable to the radiation exposure from a CT in a 1-year-old are 0.18% (abdominal) and 0.07% (head)—an order of magnitude higher than for adults—although those figures still represent a relatively small increase in cancer mortality over the natural background rate.3,4 Given the approximate 600,000 abdominal and head CT examinations performed annually in the United States on children younger than 15 years, Brennan modeling predicts that an estimated 500 persons ultimately die of cancer attributable to the CT radiation.3 Several clinical reports seem to validate the hypothetical predictions. Pearce and colleagues4 reported that the use of CT scans in children to deliver cumulative doses of approximately 50 mGy almost triples the potential risk of leukemia and doses of approximately 60 mGy triple the possible risk of brain cancer. Because these cancers are relatively rare, the cumulative absolute risks are small: in the 10 years after the first scan for patients younger than 10 years, 1 excess case of leukemia and 1 excess case of brain tumor per 10,000 head CT scans were estimated to occur. These authors advocated limiting the use of CT to situations where the clinical benefits outweigh the small absolute oncologic risks, keeping total radiation doses as low as possible, and considering alternative procedures that do not involve ionizing radiation, if possible. Other studies have reported similar increases in cancer risk with routine CT scan.5 Given these concerns, the benefit of preoperative CT in patients with NSSC is less clear. Fearon and coworkers2 were able to accurately diagnose 98% of the patients with NSSC using only clinical examination. These authors concluded that preoperative CT was generally unnecessary. In contrast, Da Silva Freitas and colleagues6 found
The Journal of Craniofacial Surgery • Volume 25, Number 4, July 2014
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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that clinical diagnosis alone provided an inaccurate or incomplete diagnosis in 7% of the patients with single suture fusion. Moreover, they observed intracranial pathology in 8 of the 89 patients. These authors support the use of preoperative CT imaging in patients with NSSC to improve diagnostic accuracy and to detect incidental findings that may require referral or result in a change in management. In the face of these contrasting reports, we sought to determine (1) the reliability of clinical diagnosis in patients with NSSC. (2) the rate of incidental CT findings, and (3) if any incidental findings would impact perioperative or postoperative management.
MATERIALS AND METHODS We performed a retrospective analysis of all patients undergoing cranial vault remodeling at our institution between 1999 and 2011. Inclusion criteria were (1) CT-verified NSSC and (2) preoperative high-resolution head CT scan available for review. The CT images were reviewed by 3 pediatric neurosurgeons blinded to the patient diagnosis and official radiology report. Each documented the site of synostosis and any other radiographic findings. An incidental finding was defined as a finding that was anomalous or out of the range of normal as perceived by a radiologist or neurosurgeon. They also opined as to whether the incidental finding would lead to a change in perioperative or postoperative management (eg, additional evaluation, intervention, or referral).
RESULTS Of the 234 patients who underwent cranial vault remodeling for various forms of craniosynostosis, 80 patients met the inclusion criteria. Mean age at CT was 6.9 months, and 68.8% of the patients were men. No significant differences were documented between patient groups. Sites of synostosis included sagittal (n = 51), coronal (n = 17), metopic (n = 11), and frontosphenoidal (n = 1). Clinical diagnosis correlated with radiographic site of fusion in all patients except for the patient with frontosphenoidal synostosis. Incidental findings were documented in more than 50% of the patients (Table 1, Fig. 1), most commonly being prominent extra-axial cerebrospinal fluid (CSF). Incidental findings that necessitated further workup or management included the patient with a Chiari malformation for whom subsequent magnetic resonance imaging (MRI) was recommended and 4 patients with ventriculomegaly that required follow-up head circumference or repeat CT.
DISCUSSION Our findings further confirm that most forms of single suture craniosynostosis can be accurately diagnosed by clinical examination alone; only 1 of the 80 patients was incorrectly diagnosed, and this was in a relatively rare form of sutural fusion (isolated frontosphenoidal craniosynostosis).7,8 With an exception, preoperative CT added no additional diagnostic information regarding the site of synostosis and was unnecessary to confirm the presence or TABLE 1. Incidental Findings on Preoperative CT
Findings Prominent extra-axial CSF Ventriculomegaly Choroid fissure cyst Cavum septum pellucidum Chiari malformation Prominent perivascular space
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Patients
Total Patients, %
Total Incidental Findings, %
36 5 2 2 1 1
45 6.25 2.5 2.5 1.25 1.25
78 11 4.35 4.35 2.2 2.2
FIGURE 1. Incidental findings on preoperative CT. A, Ventriculomegaly. B, Prominent frontal CSF. C, Chiari malformation on CT. D, Chiari malformation on subsequent MRI scan.
location of a cranial fusion. This aspect of our findings is similar to those of Fearon and coworkers2 but in contrast to the findings of Da Silva Freitas and colleagues6 who found that preoperative CT clarified or changed clinical diagnosis in 7% of their patients. The reason for these contrasting study results is unclear, but many centers still order preoperative CT scan for diagnostic confirmation, evaluation of the cerebral ventricles, and operative planning6,9–12 Although we do not routinely use CT for preoperative planning, several large centers advocate this approach to yield better clinical results.13,14 Although preoperative CT was not necessary to make or clarify the diagnosis in nearly all of our patients with NSSC, we found a relatively high rate of incidental findings that support the use of some form of preoperative intracranial imaging. More than 50% of our patients had an abnormal finding on CT scan, including 6.25% that required some type of additional clinical or radiographic follow-up. Previous studies that evaluated incidental findings found on pediatric cranial CT scans found a 4% to 26%15,16 rate of incidental findings on 1 study,15 showing 1% requiring further intervention or follow-up. Thus, our study demonstrated an even higher rate of incidental findings in the craniosynostosis population. Most of the incidental findings in our study were that of benign extra-axial fluid (also referred to as benign external hydrocephalus), which was present in almost half of our patients (45%). Our panel of neurosurgeons expressed doubt that preoperative knowledge of this condition would have significantly changed perioperative management. Nevertheless, various reports of patients with external hydrocephalus who have gone on to develop spontaneous subdural hematoma17,18 have led to the common perception that distention of the subarachnoid space may predispose patients to subdural bleeding, thereby prompting pediatric neurosurgeons at the University of Chicago to develop a mathematical model that predicted an increased frequency of venous stretch injury and bleeding in patients with widened extra-axial space, after even a minor head trauma.19 It is possible © 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 4, July 2014
that the presence of benign extra-axial CSF in patients undergoing cranial remodeling for NSSC may predispose them to an increased risk of subdural bleeding. Whereas the decision to operate and the technique used are unlikely to change as a result of such information, the presence of increased extra-axial fluid may be exculpatory if such an event occurs in the perioperative period. Our findings are consistent with the work of Da Silva Freitas and coworkers,6 who found potential significant incidental intracranial findings in 8% of their patients with NSSC. Of the significant findings identified, the authors did not comment on whether this altered perioperative or postoperative management. These authors concluded that preoperative CT provided greater diagnostic accuracy and timely detection of concurrent congenital anomalies. The clinical utility of preoperative CT to confirm the diagnosis of NSSC and/or to detect concurrent and potentially significant incidental findings must be weighed against the potential increased risk of malignancy and the added cost of the study. The increased risk of malignancy associated with ionizing radiation has been known for more than a century after reports of cancer developing in irradiated wounds and lesions (once a treatment) and elevated leukemia prevalence in radiation workers of the early 20th century.20 Further evidence of radiation-induced malignancy was derived from long-term patient follow-up after the atomic bomb explosions in Hiroshima and Nagasaki, and these data prompted some researchers to hypothesize that medical imaging could have a similar deleterious effect. On the basis of linear no-threshold modeling derived from observations in atomic bomb survivors, Brenner and Hall3 estimated that 1.5% to 2% of all malignancies in 2007 were because of CT-associated radiation. A 2009 study proposed that 29,000 additional cancers and 14,500 additional cancer deaths can be attributed to CT imaging.21 The theoretical studies of CT-related malignancy based on the linear no-threshold modeling have been criticized as unrealistic because they use data from atomic bomb survivors exposed to very high doses of radiation (mean, 200 mSv) to extrapolate the cancer risk associated with relatively low-dose (2 mSv for standard head CT) medical imaging.22,23 Nevertheless, the deleterious effects of radiation are inversely correlated with age at exposure, and children with NSSC typically undergo preoperative CT imaging very early in infancy.24 Moreover, the greater life expectancy of children results in a higher risk for eventually expressing radiation-associated injuries.25 Recent clinical studies show a statistical increase in the risk of cancer associated with childhood exposure to CT scan.4,5 This problem is especially concerning when the initial study is obtained at a center that does not adjust its CT setting to account for the age and size of the patients26 and the infant is exposed to radiation doses of around 2 mSv or the equivalent of 100 standard chest x-rays or 243 days of normal background radiation.27 Preoperative MRI avoids the radiation risks associated with CT yet allows the assessment of intracranial pathology. This imaging modality also provides excellent soft tissue definition and would be very helpful in identifying intracranial pathology, but it is relatively ineffective in evaluating suture patency.28 Anesthesia is almost always required to obtain clear images in infants and young children, and this requirement raises concerns about anesthesia-induced neural apoptosis. Animal studies have revealed potential long-term implications for children after general anesthesia.29–31 In a murine model, neonatal surgery under isoflurane resulted in neural apoptosis and neurodevelopmental impairment31; similar results were documented with the use of ketamine in rats and rhesus monkeys.30,32 Newer, more rapid MRI protocols and equipment may reduce this concern by obviating the need for anesthesia, but such techniques yield less robust images and are not widely available. Our hospital offers a “fast shunt” neurologic MRI protocol that takes 5 to 10 minutes to complete and does not require sedation in infants. The resolution and number of images is limited, but the study permits visualization of enlarged
Preoperative CT for Craniosynostosis
ventricles, benign extra-axial fluid, and larger anomalies. Finally, MRI is considerably more expensive (especially if anesthesia is required) than CT. There are several limitations of our study. First, the study is retrospective and has all of the limitations therein. However, the primary outcome measures of the study, that is, the accuracy of clinical diagnosis in patients with NSSC and the incidence of incidental CT findings in this population, should not be affected by its design. Second, the study power was reduced by a significant number of patients with inadequate or unavailable images; however, it is doubtful that a larger number of patients would have led to different results. Finally, each CT was evaluated by only 1 pediatric neurosurgeon, and intersurgeon variability was not examined in our study. Consequently, it is possible that the examiners could disagree regarding the implication of the incidental findings and/or the need for further management.
CONCLUSIONS Although preoperative CT was not necessary to clarify the diagnosis of NSSC in our patients, most of the patients were found to have concomitant findings on preoperative CT, and more than 6% warranted further evaluation or imaging. The decision to obtain preoperative CT in patients with NSSC must balance the risks of radiation exposure against the value of additional information that the study may provide. We submit that the information derived from preoperative CT may justify the small associated risks.
REFERENCES 1. Persing JA, Jane JA, Shaffrey M. Virchow and the pathogenesis of craniosynostosis: a translation of his original work. Plast Reconstr Surg 1989;83:738–742 2. Fearon JA, Singh DJ, Beals SP, et al. The diagnosis and treatment of single-sutural synostosis: are computed tomographic scans necessary? Plast Reconstr Surg 2007;120:1327–1331 3. Brenner DJ, Hall EJ. Cancer risks from CT scans: now we have data, what next? Radiology 2012;265:330–331 4. Pearce MS, Salotti JA, Little MP, et al. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet 2012;380:499–505 5. Mathews JD, Forsythe AV, Brady Z, et al. Cancer risk in 680 000 people exposed to computed tomography scans in childhood or adolescence: data linkage study of 11 million Australians. BMJ 2013;346:f2360 6. Da Silva Freitas R, de Freitas Azzolini T, Shin JH, et al. Associated (parallel) tomographic findings in patients with single-sutural synostosis. J Craniofac Surg 2010;21:411–413 7. Rogers GF, Proctor MR, Mulliken JB. Unilateral fusion of the frontosphenoidal suture: a rare cause of synostotic frontal plagiocephaly. Plast Reconstr Surg 2002;110:1011–1021 8. Sauerhammer T, Oh AK, Boyajian M, et al. Isolated frontosphenoidal synostosis: a rare cause of synostotic frontal plagiocephaly. J Neurosurg Pediatr 2014;13:553–558 9. Boyle C, Rosenblum JD. Three-dimensional CT for pre- and postsurgical imaging of patients with craniosynostosis: correlation of operative procedure and radiologic imaging. AJR Am J Roentgenol 1997;169:1173–1177 10. Posnick JC, Bite U, Nakano P, et al. Indirect intracranial volume measurements using CT scans: clinical applications for craniosynostosis. Plast Reconstr Surg 1992;89:34–45 11. Girod S, Teschner M, Schrell U, et al. Computer-aided 3-D simulation and prediction of craniofacial surgery: a new approach. J Craniomaxillofac Surg 2001;29:156–158 12. Rodt T, Schlesinger A, Schramm A, et al. 3D visualization and simulation of frontoorbital advancement in metopic synostosis. Childs Nerv Syst 2007;23:1313–1317
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13. Danelson KA, Gordon ES, David LR, et al. Using a three dimensional model of the pediatric skull for pre-operative planning in the treatment of craniosynostosis—biomed 2009. Biomed Sci Instrum 2009;45:358–363 14. Saber NR, Phillips J, Looi T, et al. Generation of normative pediatric skull models for use in cranial vault remodeling procedures. Childs Nerv Syst 2012;28:405–410 15. Rogers AJ, Maher CO, Schunk JE, et al. Incidental findings in children with blunt head trauma evaluated with cranial CT scans. Pediatrics 2013;132:e356–e363 16. Ortega HW, Vander Velden H, Reid S. Incidental findings on computed tomography scans in children with mild head trauma. Clin Pediatr (Phila) 2012;51:872–876 17. Amodio J, Spektor V, Pramanik B, et al. Spontaneous development of bilateral subdural hematomas in an infant with benign infantile hydrocephalus: color Doppler assessment of vessels traversing extra-axial spaces. Pediatr Radiol 2005;35:1113–1117 18. Swift D, McBride L. Chronic subdural hematoma in children. Neurosurg Clin N Am 2000;11:439–443 19. Papasian NC, Frim DM. A theoretical model of benign external hydrocephalus that predicts a predisposition towards extra-axial hemorrhage after minor head trauma. Pediatr Neurosurg 2000;33:188–193 20. Upton AC. Historical perspectives on radiation carcinogenesis. In: Upton AC, Albert RE, Burns FJ, et al., eds. Radiation Carcinogenesis. New York: Elsevier, 1986:1–10 21. Berrington de González A, Mahesh M, Kim KP, et al. Projected cancer risks from computed tomographic scans performed in the United States in 2007. Arch Intern Med 2009;169:2071–2077 22. Preston DL, Shimizu Y, Pierce DA, et al. Studies of mortality of atomic bomb survivors. Report 13: solid cancer and noncancer disease mortality: 1950–1997. Radiat Res 2003;160:381–407
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23. Hendee WR, O'Connor MK. Radiation risks of medical imaging: separating fact from fantasy. Radiology 2012;264:312–321 24. Wakeford R. The cancer epidemiology of radiation. Oncogene 2004;23:6404–6428 25. Chodick G, Ronckers CM, Shalev V, et al. Excess lifetime cancer mortality risk attributable to radiation exposure from computed tomography examinations in children. Isr Med Assoc J 2007;9:584–587 26. Huda W. Effective doses to adult and pediatric patients. Pediatr Radiol 2002;32:272–279 27. Mettler FA Jr, Huda W, Yoshizumi TT, et al. Effective doses in radiology and diagnostic nuclear medicine: a catalog. Radiology 2008;248:254–263 28. Eley KA, Sheerin F, Taylor N, et al. Identification of normal cranial sutures in infants on routine magnetic resonance imaging. J Craniofac Surg 2013;24:317–320 29. Viberg H, Ponten E, Eriksson P, et al. Neonatal ketamine exposure results in changes in biochemical substrates of neuronal growth and synaptogenesis, and alters adult behavior irreversibly. Toxicology 2008;249:153–159 30. Brambrink AM, Evers AS, Avidan MS, et al. Ketamine-induced neuroapoptosis in the fetal and neonatal rhesus macaque brain. Anesthesiology 2012;116:372–384 31. Zhu C, Gao J, Karlsson N, et al. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J Cereb Blood Flow Metab 2010;30:1017–1030 32. Bai X, Yan Y, Canfield S, et al. Ketamine enhances human neural stem cell proliferation and induces neuronal apoptosis via reactive oxygen species-mediated mitochondrial pathway. Anesth Analg 2013;116:869–880
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Incidental Findings on Preoperative Computed Tomography for Nonsyndromic Single Suture Craniosynostosis Keshav T. Magge, MD, Suresh N. Magge, MD, Robert F. Keating, MD, John S. Myseros, MD, Michael J. Boyajian, MD, Tina M. Sauerhammer, MD, Gary F. Rogers, MD, JD, and Albert K. Oh, MD Abstract: Although the diagnosis of nonsyndromic single suture craniosynostosis (NSSC) can usually be made by clinical examination, computed tomography (CT) is still commonly used in preoperative evaluation. This practice has been questioned in light of recent studies that document a small, but measurable, increased risk of malignancy from CT-associated radiation. The purpose of this study was to examine whether preoperative CT for patients with NSSC provided clinically important information beyond confirmation of craniosynostosis. We performed a retrospective analysis of all patients with NSSC undergoing cranial vault remodeling at our center from March 1999 to March 2011. Only patients with complete preoperative CT scans available for review were included. Staff pediatric neurosurgeons were blinded to patient diagnosis and official radiology report, analyzed the CT images, and documented the site of synostosis and any other findings. Of the 231 patients, 80 met the inclusion criteria. Sites of synostosis included sagittal (51 patients), coronal (17 patients), metopic (11 patients), and frontosphenoidal (1 patient). Clinical diagnosis correlated with radiographic site of fusion in all patients except the patient with frontosphenoidal synostosis. Incidental findings were documented in more than 50% of the patients including prominent extra-axial cerebrospinal fluid (n = 36, 45%), ventriculomegaly (n = 5, 6.25%), choroid fissure cyst (n = 2), cavum septum pellucidum (n = 2), Chiari malformation (n = 1), and prominent perivascular space (clinically nonsignificant finding, n = 1). Incidental findings required additional follow-up or management in 5 patients (6.25%). Our findings support the use of preoperative imaging in this population to identify intracranial anomalies that cannot be discerned
From the Division of Plastic and Reconstructive Surgery and the Division of Neurosurgery, Children's National Medical Center, George Washington University. Received December 17, 2013. Accepted for publication January 17, 2014. Address correspondence and reprint requests to Albert K. Oh, MD, Children's National Medical Center, 111 Michigan Ave, NW, Washington, DC 20010; E-mail: [email protected] Presented in part at the 12th International Congress on Cleft Lip/Palate and Related Craniofacial Anomalies, May 2013, and at the International Society of Craniofacial Surgery, 15th Biennial Meeting, September 2013. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000797
by clinical examination. Whereas many findings were not clinically important, some required additional attention. Key Words: Preoperative evaluation, craniosynostosis, incidental radiologic findings (J Craniofac Surg 2014;25: 1327–1330)
M
ore than 150 years ago, Virchow proposed that fusion of cranial sutures produced predictable changes in cranial shape.1 The natural corollary of this hypothesis is that most forms of single suture craniosynostosis can be diagnosed by clinical examination. This tenet is nearly universally accepted, yet confirmatory computed tomography (CT) scan is still the standard practice in most centers. Opponents of routine diagnostic CT evaluation for nonsyndromic single suture craniosynostosis (NSSC) suggest that the test is rarely required to make the diagnosis, adds to the cost of delivering care, and occasionally requires general anesthesia.2 Their argument is further reinforced by a series of recent reports highlighting the deleterious effects of ionizing radiation on infants. Brenner and Hall3 showed that the estimated lifetime cancer mortality risks attributable to the radiation exposure from a CT in a 1-year-old are 0.18% (abdominal) and 0.07% (head)—an order of magnitude higher than for adults—although those figures still represent a relatively small increase in cancer mortality over the natural background rate.3,4 Given the approximate 600,000 abdominal and head CT examinations performed annually in the United States on children younger than 15 years, Brennan modeling predicts that an estimated 500 persons ultimately die of cancer attributable to the CT radiation.3 Several clinical reports seem to validate the hypothetical predictions. Pearce and colleagues4 reported that the use of CT scans in children to deliver cumulative doses of approximately 50 mGy almost triples the potential risk of leukemia and doses of approximately 60 mGy triple the possible risk of brain cancer. Because these cancers are relatively rare, the cumulative absolute risks are small: in the 10 years after the first scan for patients younger than 10 years, 1 excess case of leukemia and 1 excess case of brain tumor per 10,000 head CT scans were estimated to occur. These authors advocated limiting the use of CT to situations where the clinical benefits outweigh the small absolute oncologic risks, keeping total radiation doses as low as possible, and considering alternative procedures that do not involve ionizing radiation, if possible. Other studies have reported similar increases in cancer risk with routine CT scan.5 Given these concerns, the benefit of preoperative CT in patients with NSSC is less clear. Fearon and coworkers2 were able to accurately diagnose 98% of the patients with NSSC using only clinical examination. These authors concluded that preoperative CT was generally unnecessary. In contrast, Da Silva Freitas and colleagues6 found
The Journal of Craniofacial Surgery • Volume 25, Number 4, July 2014
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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that clinical diagnosis alone provided an inaccurate or incomplete diagnosis in 7% of the patients with single suture fusion. Moreover, they observed intracranial pathology in 8 of the 89 patients. These authors support the use of preoperative CT imaging in patients with NSSC to improve diagnostic accuracy and to detect incidental findings that may require referral or result in a change in management. In the face of these contrasting reports, we sought to determine (1) the reliability of clinical diagnosis in patients with NSSC. (2) the rate of incidental CT findings, and (3) if any incidental findings would impact perioperative or postoperative management.
MATERIALS AND METHODS We performed a retrospective analysis of all patients undergoing cranial vault remodeling at our institution between 1999 and 2011. Inclusion criteria were (1) CT-verified NSSC and (2) preoperative high-resolution head CT scan available for review. The CT images were reviewed by 3 pediatric neurosurgeons blinded to the patient diagnosis and official radiology report. Each documented the site of synostosis and any other radiographic findings. An incidental finding was defined as a finding that was anomalous or out of the range of normal as perceived by a radiologist or neurosurgeon. They also opined as to whether the incidental finding would lead to a change in perioperative or postoperative management (eg, additional evaluation, intervention, or referral).
RESULTS Of the 234 patients who underwent cranial vault remodeling for various forms of craniosynostosis, 80 patients met the inclusion criteria. Mean age at CT was 6.9 months, and 68.8% of the patients were men. No significant differences were documented between patient groups. Sites of synostosis included sagittal (n = 51), coronal (n = 17), metopic (n = 11), and frontosphenoidal (n = 1). Clinical diagnosis correlated with radiographic site of fusion in all patients except for the patient with frontosphenoidal synostosis. Incidental findings were documented in more than 50% of the patients (Table 1, Fig. 1), most commonly being prominent extra-axial cerebrospinal fluid (CSF). Incidental findings that necessitated further workup or management included the patient with a Chiari malformation for whom subsequent magnetic resonance imaging (MRI) was recommended and 4 patients with ventriculomegaly that required follow-up head circumference or repeat CT.
DISCUSSION Our findings further confirm that most forms of single suture craniosynostosis can be accurately diagnosed by clinical examination alone; only 1 of the 80 patients was incorrectly diagnosed, and this was in a relatively rare form of sutural fusion (isolated frontosphenoidal craniosynostosis).7,8 With an exception, preoperative CT added no additional diagnostic information regarding the site of synostosis and was unnecessary to confirm the presence or TABLE 1. Incidental Findings on Preoperative CT
Findings Prominent extra-axial CSF Ventriculomegaly Choroid fissure cyst Cavum septum pellucidum Chiari malformation Prominent perivascular space
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Patients
Total Patients, %
Total Incidental Findings, %
36 5 2 2 1 1
45 6.25 2.5 2.5 1.25 1.25
78 11 4.35 4.35 2.2 2.2
FIGURE 1. Incidental findings on preoperative CT. A, Ventriculomegaly. B, Prominent frontal CSF. C, Chiari malformation on CT. D, Chiari malformation on subsequent MRI scan.
location of a cranial fusion. This aspect of our findings is similar to those of Fearon and coworkers2 but in contrast to the findings of Da Silva Freitas and colleagues6 who found that preoperative CT clarified or changed clinical diagnosis in 7% of their patients. The reason for these contrasting study results is unclear, but many centers still order preoperative CT scan for diagnostic confirmation, evaluation of the cerebral ventricles, and operative planning6,9–12 Although we do not routinely use CT for preoperative planning, several large centers advocate this approach to yield better clinical results.13,14 Although preoperative CT was not necessary to make or clarify the diagnosis in nearly all of our patients with NSSC, we found a relatively high rate of incidental findings that support the use of some form of preoperative intracranial imaging. More than 50% of our patients had an abnormal finding on CT scan, including 6.25% that required some type of additional clinical or radiographic follow-up. Previous studies that evaluated incidental findings found on pediatric cranial CT scans found a 4% to 26%15,16 rate of incidental findings on 1 study,15 showing 1% requiring further intervention or follow-up. Thus, our study demonstrated an even higher rate of incidental findings in the craniosynostosis population. Most of the incidental findings in our study were that of benign extra-axial fluid (also referred to as benign external hydrocephalus), which was present in almost half of our patients (45%). Our panel of neurosurgeons expressed doubt that preoperative knowledge of this condition would have significantly changed perioperative management. Nevertheless, various reports of patients with external hydrocephalus who have gone on to develop spontaneous subdural hematoma17,18 have led to the common perception that distention of the subarachnoid space may predispose patients to subdural bleeding, thereby prompting pediatric neurosurgeons at the University of Chicago to develop a mathematical model that predicted an increased frequency of venous stretch injury and bleeding in patients with widened extra-axial space, after even a minor head trauma.19 It is possible © 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 4, July 2014
that the presence of benign extra-axial CSF in patients undergoing cranial remodeling for NSSC may predispose them to an increased risk of subdural bleeding. Whereas the decision to operate and the technique used are unlikely to change as a result of such information, the presence of increased extra-axial fluid may be exculpatory if such an event occurs in the perioperative period. Our findings are consistent with the work of Da Silva Freitas and coworkers,6 who found potential significant incidental intracranial findings in 8% of their patients with NSSC. Of the significant findings identified, the authors did not comment on whether this altered perioperative or postoperative management. These authors concluded that preoperative CT provided greater diagnostic accuracy and timely detection of concurrent congenital anomalies. The clinical utility of preoperative CT to confirm the diagnosis of NSSC and/or to detect concurrent and potentially significant incidental findings must be weighed against the potential increased risk of malignancy and the added cost of the study. The increased risk of malignancy associated with ionizing radiation has been known for more than a century after reports of cancer developing in irradiated wounds and lesions (once a treatment) and elevated leukemia prevalence in radiation workers of the early 20th century.20 Further evidence of radiation-induced malignancy was derived from long-term patient follow-up after the atomic bomb explosions in Hiroshima and Nagasaki, and these data prompted some researchers to hypothesize that medical imaging could have a similar deleterious effect. On the basis of linear no-threshold modeling derived from observations in atomic bomb survivors, Brenner and Hall3 estimated that 1.5% to 2% of all malignancies in 2007 were because of CT-associated radiation. A 2009 study proposed that 29,000 additional cancers and 14,500 additional cancer deaths can be attributed to CT imaging.21 The theoretical studies of CT-related malignancy based on the linear no-threshold modeling have been criticized as unrealistic because they use data from atomic bomb survivors exposed to very high doses of radiation (mean, 200 mSv) to extrapolate the cancer risk associated with relatively low-dose (2 mSv for standard head CT) medical imaging.22,23 Nevertheless, the deleterious effects of radiation are inversely correlated with age at exposure, and children with NSSC typically undergo preoperative CT imaging very early in infancy.24 Moreover, the greater life expectancy of children results in a higher risk for eventually expressing radiation-associated injuries.25 Recent clinical studies show a statistical increase in the risk of cancer associated with childhood exposure to CT scan.4,5 This problem is especially concerning when the initial study is obtained at a center that does not adjust its CT setting to account for the age and size of the patients26 and the infant is exposed to radiation doses of around 2 mSv or the equivalent of 100 standard chest x-rays or 243 days of normal background radiation.27 Preoperative MRI avoids the radiation risks associated with CT yet allows the assessment of intracranial pathology. This imaging modality also provides excellent soft tissue definition and would be very helpful in identifying intracranial pathology, but it is relatively ineffective in evaluating suture patency.28 Anesthesia is almost always required to obtain clear images in infants and young children, and this requirement raises concerns about anesthesia-induced neural apoptosis. Animal studies have revealed potential long-term implications for children after general anesthesia.29–31 In a murine model, neonatal surgery under isoflurane resulted in neural apoptosis and neurodevelopmental impairment31; similar results were documented with the use of ketamine in rats and rhesus monkeys.30,32 Newer, more rapid MRI protocols and equipment may reduce this concern by obviating the need for anesthesia, but such techniques yield less robust images and are not widely available. Our hospital offers a “fast shunt” neurologic MRI protocol that takes 5 to 10 minutes to complete and does not require sedation in infants. The resolution and number of images is limited, but the study permits visualization of enlarged
Preoperative CT for Craniosynostosis
ventricles, benign extra-axial fluid, and larger anomalies. Finally, MRI is considerably more expensive (especially if anesthesia is required) than CT. There are several limitations of our study. First, the study is retrospective and has all of the limitations therein. However, the primary outcome measures of the study, that is, the accuracy of clinical diagnosis in patients with NSSC and the incidence of incidental CT findings in this population, should not be affected by its design. Second, the study power was reduced by a significant number of patients with inadequate or unavailable images; however, it is doubtful that a larger number of patients would have led to different results. Finally, each CT was evaluated by only 1 pediatric neurosurgeon, and intersurgeon variability was not examined in our study. Consequently, it is possible that the examiners could disagree regarding the implication of the incidental findings and/or the need for further management.
CONCLUSIONS Although preoperative CT was not necessary to clarify the diagnosis of NSSC in our patients, most of the patients were found to have concomitant findings on preoperative CT, and more than 6% warranted further evaluation or imaging. The decision to obtain preoperative CT in patients with NSSC must balance the risks of radiation exposure against the value of additional information that the study may provide. We submit that the information derived from preoperative CT may justify the small associated risks.
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Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
