Endoscopic treatment of combined metopic-sagittal craniosynostosis

Ema Zubovic MD1, Gary B. Skolnick BS1, Sybill D. Naidoo PhD, RN, CPNP1, Mark Bellanger CPed, COA, ATC3, Matthew D. Smyth MD2, and Kamlesh B. Patel MD, MSc1
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  • 1 Division of Plastic & Reconstructive Surgery, Department of Surgery, and
  • | 2 Department of Neurosurgery, Washington University School of Medicine in St. Louis; and
  • | 3 Orthotic and Prosthetic Lab, St. Louis, Missouri
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OBJECTIVE

Combined metopic-sagittal craniosynostosis is traditionally treated with open cranial vault remodeling and fronto-orbital advancement, sometimes in multiple operations. Endoscopic treatment of this multisuture synostosis presents a complex challenge for the surgeon and orthotist.

METHODS

The authors retrospectively analyzed the preoperative and 1-year postoperative CT scans of 3 patients with combined metopic-sagittal synostosis, all of whom were treated with simultaneous endoscope-assisted craniectomy of the metopic and sagittal sutures followed by helmet therapy. Established anthropometric measurements were applied to assess pre- and postoperative morphology, including cranial index and interfrontal divergence angle (IFDA). Patients’ measurements were compared to those obtained in 18 normal controls.

RESULTS

Two boys and one girl underwent endoscope-assisted craniectomy at a mean age of 81 days. The mean preoperative cranial index was 0.70 (vs control mean of 0.82, p = 0.009), corrected postoperatively to a mean of 0.82 (vs control mean of 0.80, p = 0.606). The mean preoperative IFDA was 110.4° (vs control mean of 152.6°, p = 0.017), corrected postoperatively to a mean of 139.1° (vs control mean of 140.3°, p = 0.348). The mean blood loss was 100 mL and the mean length of stay was 1.7 days. No patient underwent reoperation. The mean clinical follow-up was 3.4 years.

CONCLUSIONS

Endoscope-assisted craniectomy with helmet therapy is a viable single-stage treatment option for combined metopic-sagittal synostosis, providing correction of the stigmata of trigonoscaphocephaly, with normalization of the cranial index and IFDA.

ABBREVIATIONS

IFDA = interfrontal divergence angle; ZF-G-ZF angle = glabella and bilateral zygomaticofrontal sutures; ZF-ZF = interzygomaticofrontal.

OBJECTIVE

Combined metopic-sagittal craniosynostosis is traditionally treated with open cranial vault remodeling and fronto-orbital advancement, sometimes in multiple operations. Endoscopic treatment of this multisuture synostosis presents a complex challenge for the surgeon and orthotist.

METHODS

The authors retrospectively analyzed the preoperative and 1-year postoperative CT scans of 3 patients with combined metopic-sagittal synostosis, all of whom were treated with simultaneous endoscope-assisted craniectomy of the metopic and sagittal sutures followed by helmet therapy. Established anthropometric measurements were applied to assess pre- and postoperative morphology, including cranial index and interfrontal divergence angle (IFDA). Patients’ measurements were compared to those obtained in 18 normal controls.

RESULTS

Two boys and one girl underwent endoscope-assisted craniectomy at a mean age of 81 days. The mean preoperative cranial index was 0.70 (vs control mean of 0.82, p = 0.009), corrected postoperatively to a mean of 0.82 (vs control mean of 0.80, p = 0.606). The mean preoperative IFDA was 110.4° (vs control mean of 152.6°, p = 0.017), corrected postoperatively to a mean of 139.1° (vs control mean of 140.3°, p = 0.348). The mean blood loss was 100 mL and the mean length of stay was 1.7 days. No patient underwent reoperation. The mean clinical follow-up was 3.4 years.

CONCLUSIONS

Endoscope-assisted craniectomy with helmet therapy is a viable single-stage treatment option for combined metopic-sagittal synostosis, providing correction of the stigmata of trigonoscaphocephaly, with normalization of the cranial index and IFDA.

ABBREVIATIONS

IFDA = interfrontal divergence angle; ZF-G-ZF angle = glabella and bilateral zygomaticofrontal sutures; ZF-ZF = interzygomaticofrontal.

In Brief

The authors present their surgical technique for endoscopic treatment of combined metopic-sagittal craniosynostosis and evaluate the head shape outcomes of 3 patients by using established measurements, comparing patients to normal controls before and after surgery. This study is the first to report outcomes of endoscopic treatment for this rare form of multisuture craniosynostosis, which is traditionally treated with 2 separate open cranial vault reconstructions.

Combined synostosis of the metopic and sagittal sutures is exceedingly rare, representing just 0.5%–2% of all craniosynostosis cases.1,2 Trigonoscaphocephaly, the result of simultaneous frontal, temporal, and biparietal growth restriction, presents a more complex reconstructive challenge than either metopic or sagittal synostosis alone. Traditional practice has been a 2-stage open surgical repair to address each synostosis separately. Czerwinski et al. suggested an initial procedure to repair the sagittal synostosis when patients are 6–8 months of age, followed by correction of the metopic synostosis by fronto-orbital advancement at 10–12 months of age, allowing for a more stable fronto-orbital bandeau reconstruction.3 More recently, Dobbs et al. published the first report of single-stage open repair for combined metopic-sagittal synostosis.1

The risk of potential surgical and anesthetic morbidity is increased with multiple open transcranial operations in the 1st year of life. For single-suture craniosynostosis, endoscopic procedures have been shown to decrease blood loss, operating time, length of hospital stay, and cost relative to open approaches.4–8 In patients with isolated metopic or sagittal synostosis, equivalent morphological outcomes have been achieved with endoscope-assisted craniectomy followed by postoperative molding helmet therapy.9–14 To our knowledge, there has been no report in the literature of single-stage endoscope-assisted craniectomy with molding helmet therapy for combined metopic-sagittal synostosis.

In this report, our aim was as follows: to 1) present our experience in endoscopic treatment of combined metopic-sagittal synostosis, demonstrating our operative technique and postoperative helmet therapy protocol; 2) objectively evaluate the postoperative morphological outcomes of patients treated endoscopically; and 3) compare these patients to normal controls as an evaluation of success in normalization of cranial and facial morphology.

Methods

After obtaining institutional review board approval, we identified 3 patients treated endoscopically for combined metopic-sagittal craniosynostosis at our institution between 2012 and 2017. All 3 underwent endoscope-assisted craniectomy performed by the same craniofacial surgeon (K.B.P.) and neurosurgeon (M.D.S.), followed by custom molding helmet therapy until 1 year of age.

Preoperative Evaluation

After preoperative evaluation by both treating surgeons, patients underwent preoperative low-dose CT imaging to confirm the clinical diagnosis of metopic-sagittal craniosynostosis. Our practice is to offer both open and endoscopic treatment options to eligible patients younger than 5 months of age, and only open treatment to older patients. We prefer patients to be 2–3 months of age for endoscopic treatment to allow the orthotist to take advantage of the rapid skull growth of early infancy.14,15 Endoscopic treatment of multisuture synostosis places more complex demands on postoperative molding helmet therapy, which are best met by early initiation of helmet therapy. Patients meet the orthotist and undergo scanning for a custom molding helmet in the week before surgery, in order to ensure helmet availability in the immediate postoperative period.

Operative Technique

We initially performed this procedure with the patient entirely in the prone sphinx position, but our preferred technique is now to complete the metopic suturectomy with the patient supine, repositioning to the sphinx position for the sagittal suturectomy. This allows for more complete visualization and more facile instrumentation for each approach. We have previously published examples of patient positioning for endoscopic repairs of metopic14 and sagittal13 synostosis.

Metopic Suturectomy

The patient is positioned supine, with the head elevated in a Mayfield headrest above the level of the heart to minimize blood loss. Intravenous dexamethasone and tranexamic acid are administered. After sterile preparation, draping, and infiltration of local anesthesia, a 2.5-cm transverse incision is made in the frontal hairline, and subgaleal dissection is extended to the levels of the nasofrontal suture and the anterior fontanelle. A burr hole is made through the fused metopic suture at the level of the skin incision, and is then widened and extended posteriorly. A 1-cm-wide strip craniectomy of the fused metopic suture is performed with Tessier bone scissors (KLS Martin) to the level of the anterior fontanelle. Bone edges are coagulated using 50-W monopolar suction electrocautery, illuminated by a lighted rhinoplasty retractor, and with coated malleable retractors (Karl Storz) protecting the dura mater. Care is taken to remove the bone in segments after controlling any emissary veins with bipolar electrocautery. The anterior remainder of the fused metopic suture is resected, tapering to the level of the nasofrontal suture. The majority of the 1-cm strip craniectomy is done under direct visualization. Completion of suturectomy is confirmed by endoscopic visualization of the nasal upper lateral cartilages (Fig. 1), the tips of which are seen at the nasofrontal junction under the nasal bones. The nasal bones are not resected. Floseal (Baxter International) is placed in the craniectomy defect. The skin incision is closed in layered fashion with resorbable suture and skin glue.

FIG. 1.
FIG. 1.

Intraoperative endoscopic image showing completion of metopic suturectomy with visualization of nasal upper lateral cartilages (ULC). The cranial extent of the upper lateral cartilages indicates the level of the nasofrontal suture in an infant (see Poublon et al.29), confirming complete metopic suturectomy. Figure is available in color online only.

Sagittal Suturectomy

After completion of the metopic suturectomy and skin closure, the patient is repositioned in the sphinx position and sterile preparation and draping is repeated. Hair is clipped, and 2 new 2.5-cm transverse incisions are made just posterior to the anterior fontanelle and just anterior to lambda. Subgaleal dissection is again extended across the fused sagittal suture, connecting the 2 access incisions. Burr holes are made to the side of the fused sagittal suture through each access incision, then widened with curettes and Kerrison punches, and osteotomies are extended across midline. After mobilization of the dura, the wedge of cranial bone between the anterior osteotomy and the posterior aspect of the anterior fontanelle is excised under direct visualization with Tessier bone scissors. An endoscope is introduced into the epidural space posteriorly, and the dura is dissected from the inner table. A 2-cm-wide segment of the fused sagittal suture is excised with paramedian cuts by using Tessier bone scissors and extracted through the anterior incision. Finally, the remaining bone anterior to lambda is freed and excised. Bone edges are again coagulated with suction electrocautery, under visualization by 0° endoscope. Floseal is again placed in the craniectomy defect and access incisions are closed in the same fashion as above.

Patients without significant comorbidities are typically admitted overnight to a regular surgical ward and hematocrit is measured 4 hours postoperatively. Discharge home on postoperative day 1 is standard. Patients using a local orthotist are typically fitted with their helmet prior to hospital discharge; those using a more distant orthotic company have a helmet fitting appointment within the first 3 postoperative days. Edema control with head elevation and 24 hours of intravenous dexamethasone (beginning with the intraoperative dose) are essential to allow early helmet fitting.

Helmet Therapy

We recommend 23 hours of helmet wear daily until patients are 12 months of age, when 65% of brain growth is complete.14,16 Orthotist visits occur every 1–2 weeks initially, and then every 3–4 weeks as the child gets older—for serial measurements and helmet adjustments as needed. The need for fabrication of a new helmet is determined primarily by head growth, and the number of helmets a patient will require is dependent on the rate and amount of head growth during treatment. The 3 patients presented here were treated with 3, 5, and 4 postoperative molding helmets, respectively, over the course of their 1st year of life. This reflects our trend over the past decade toward more aggressive head shape correction in the early postoperative months for all endoscopic synostosis repairs, reducing the maximum treatment period of each helmet before a new one becomes necessary.17

Data Collection

Three-dimensionally reconstructed preoperative and 1-year postoperative CT scans were studied using Analyze 12.0 image analysis software (Mayo Clinic). Each scan was oriented to the Frankfort horizontal plane.18 Established anthropometric measurements for isolated metopic and sagittal synostosis were applied to assess pre- and postoperative morphology, with scans set to bone or soft-tissue thresholds as appropriate. The severity of scaphocephaly was measured using cranial index19 on a bone threshold. Trigonocephaly was quantified by the angle formed by the glabella and bilateral zygomaticofrontal sutures (ZF-G-ZF angle) based on Kellogg et al.20 (Fig. 2) and by the interfrontal divergence angle (IFDA) as defined by Wood et al.21 (Fig. 3), both on bone thresholds. Interorbital width was defined by the interzygomaticofrontal (ZF-ZF) distance on bone thresholds, and intercanthal distance was measured on soft-tissue thresholds, both to the nearest 0.5 mm.14

FIG. 2.
FIG. 2.

The ZF-G-ZF angle. Angle (red solid line) formed by glabella (solid red circles) and bilateral zygomaticofrontal sutures (open and solid orange circles), projected onto a single axial plane (red dashed line) parallel to the Frankfort horizontal. Originally defined by Kellogg et al.20 and reported in Nguyen et al.14 Figure is available in color online only.

FIG. 3.
FIG. 3.

The IFDA as defined by Wood et al.21 On a CT scan oriented to the axial plane containing the opisthion (large yellow circle) and superior-most points of the clinoid processes of the dorsum sellae (small yellow circles), a triangle (orange line) is formed between the anterior-most point of the cranium and the exterior of bilateral coronal sutures. Perpendicular bisectors (orange dashed lines) intersect with the outermost aspect of the frontal bones (red circles). The IFDA (red line) is the angle between these points and the anterior-most point. Figure is available in color online only.

For each patient scan, 3 age- and sex-matched control scans were selected from a database of head CTs performed at our institution between 2000 and 2013 for reasons other than suspected craniosynostosis (e.g., trauma, seizure). The measurements listed above were also taken on reconstructions of these normal control scans. The mean values from each trio of control scans were calculated and matched with the related case-scan measures for analysis. Age matching resulted in a mean preoperative CT age difference of 7 days (range 1–25 days) and a mean postoperative CT age difference of 19 days (range 3–41 days) between cases and controls.

The patient in case 1 had an additional follow-up CT scan at 5 years postoperatively. We have since stopped routinely obtaining 5-year CT scans due to limited clinical utility and to minimize radiation exposure, but we present this patient’s 5-year measurements as an evaluation of durability of the early postoperative result. The same 5 measurements were taken on this CT scan as above and were compared to the same patient’s 1-year postoperative measurements and to 3 additional age- and sex-matched control scans (mean age difference 157 days, range 117–216 days).

Patient charts were reviewed for demographic data, head circumference at each visit, operative duration, estimated blood loss, transfusion requirement, hospital length of stay, postoperative complications, reoperations, and duration of follow-up. Paired Student t-tests were used to compare cases to controls. All statistical analysis was done using IBM SPSS Statistics software, version 23 (IBM Corp.).

Results

Two boys and one girl underwent repair at the mean age of 81 days (range 68–98 days). The mean estimated blood loss was 100 mL (range 70–150 mL), and all 3 patients received intraoperative transfusion (mean 108 mL, range 100–125 mL). The mean operating time (incision to closure) was 131 minutes (range 120–148 minutes). The only postoperative complication was a seizure in the postanesthesia care unit in 1 patient, which ceased after 3 doses of lorazepam. This patient was subsequently admitted to the intensive care unit for monitoring, with no further seizure activity, normal findings on CT and MR images of the brain, and unremarkable electroencephalography findings. The patient was discharged on postoperative day 3. The other 2 patients were discharged on postoperative day 1 after uneventful overnight stays. The mean postoperative clinical follow-up was 3.4 years (range 1.1–7.6 years).

Anthropometric measurements are shown in Table 1. Preoperatively, study patients had a significantly smaller cranial index, ZF-G-ZF angle, IFDA, and intercanthal distance relative to controls (p ≤ 0.046). There was no significant difference between study patients and controls in any of the 5 measures postoperatively (p ≥ 0.225). Figure 4 shows pre- and postoperative comparisons between patients and controls. Head circumferences for all 3 patients followed normal growth curves throughout the follow-up period.

TABLE 1.

Preoperative and postoperative measurements in pediatric patients with combined metopic-sagittal craniosynostosis

Preop ValuesPostop Values
MeasurementCase 1Case 2Case 3Patient MeanControl Meanp Value95% CI*Case 1Case 2Case 3Patient MeanControl Meanp Value95% CI*
Age at CT (days)3728541430.661−20, 164255825075045010.701−31, 38
Cranial index0.690.720.680.700.820.009−0.17, −0.070.810.800.870.820.800.606−0.13, 0.17
ZF-G-ZF angle104.6°89.4°82.1°92.1°130.1°0.046−74.6°, −1.5°130.2°125.2°124.3°126.6°128.4°0.350−8.1°, 4.6°
IFDA119.8°113.9°97.6°110.4°152.6°0.017−66.1°, −18.3°141.8°136.9°138.5°139.1°140.3°0.348−5.3°, 3.0°
Intercanthal distance (mm)23.020.022.021.724.30.028−4.5, −0.726.527.028.527.328.10.677−7.2, 5.7
ZF-ZF distance (mm)61.551.051.054.565.00.112−27.1, 6.176.577.072.075.276.20.225−3.5, 1.5

95% CI of the difference of the means.

Indicates statistically significant difference between patients and controls.

FIG. 4.
FIG. 4.

Scatterplots showing anthropometric comparisons; pre- and postoperative values are shown. Study patients with metopic-sagittal synostosis are represented by colored triangles; age-matched controls are represented by open circles. Significant differences between study and control groups are marked with asterisks. Figure is available in color online only.

On 1-year postoperative CT scans, 2 patients had developed interval fusions of additional cranial sutures—the patient in case 1 had fusion of bilateral coronal sutures and development of a sagittal neosuture, and the patient in case 2 had partial fusion of the right coronal suture. Neither had any signs of new synostosis on physical examination, and head shape development progressed appropriately based on findings of clinical examination. All 3 patients underwent genetic evaluation and only the patient in case 3 was found to have a syndromic association. No patients underwent reoperation. There were no concerns for increased intracranial pressure in any of the patients at pre- or postoperative examinations. All made normal neurodevelopmental progress based on assessment by the craniofacial team psychologist. CT scans are shown in Fig. 5. Long-term photographic follow-up of the patient in case 1 is shown in Fig. 6.

FIG. 5.
FIG. 5.

Chronological CT scans of the 3 study patients, to scale. The patient in case 1 is noted to have a posterior calvarial indentation just anterior to lambda, a deformity previously described after repair of sagittal synostosis (see Shah et al.41). This was present preoperatively, and although it had improved on 1-year postoperative CT scan, it reappeared at 5 years. This irregularity is not noted in the other 2 patients. The patient in case 1 also developed bicoronal synostosis postoperatively. Slight orbital asymmetry and nasal root deviation are noted on 5-year postoperative CT scan. The patient in case 2 developed right unicoronal synostosis, with no notable effect on head shape or facial symmetry at 1 year.

FIG. 6.
FIG. 6.

Case 1. Chronological photographs. Helmet therapy was completed at age 12 months. Mild bitemporal retrusion improved over time. A: Preoperative photograph obtained at 5 weeks of age. B: Photograph obtained 5 months postoperatively, at 8 months of age. C: Photograph obtained 1.5 years postoperatively, at 20 months of age. D: Photograph obtained 7 years postoperatively, at 7 years of age. Figure is available in color online only.

On 5-year postoperative scan, the patient in case 1 had a cranial index of 0.81 (from 0.81 at 1 year postoperatively; 5-year control mean cranial index 0.75); a ZF-G-ZF of 135.9° (from 130.2° at 1 year; 5-year control mean ZF-G-ZF 135.6°); an IFDA of 143.1° (from 141.8° at 1 year; 5-year control mean IFDA 140.2°); an intercanthal distance of 30.6 mm (from 26.5 mm at 1 year; 5-year control mean intercanthal distance 32.0 mm); and a ZF-ZF distance of 86.8 mm (from 76.5 mm at 1 year; 5-year control mean ZF-ZF distance 90.3 mm). Minimal facial skeletal asymmetry was noted on CT scans, with slight nasal root deviation and orbital asymmetry (Fig. 5). Results of yearly ophthalmological evaluations were normal, and this patient required no ophthalmological procedures. He continued to have good neurodevelopmental progress, with no deficits on child psychology evaluation.

Discussion

Although techniques of craniosynostosis repair continue to evolve, from refinements in traditional open cranial vault remodeling to the development of less-invasive techniques, the goals remain unchanged—to achieve a normal head shape and relieve restrictions on head growth imposed by premature sutural fusion.22 For isolated metopic or sagittal synostoses, previous studies have demonstrated equivalent outcomes in head shape correction with endoscope-assisted craniectomy and molding helmet therapy relative to open reconstructions.10–14 Successful endoscopic treatment of various multisuture synostoses has been reported,23 but there are no specific outcomes of endoscopic treatment of combined metopic-sagittal synostosis documented in the literature. In this study we report the anthropometric outcomes of 3 patients treated with single-stage endoscope-assisted craniectomy and postoperative molding helmet therapy and compare their measurements to those of age-matched normal controls.

The presence of concomitant metopic synostosis restricts the typical frontal bossing of sagittal synostosis, causing a seemingly less obvious scaphocephalic head shape,1,24,25 but biparietal growth restriction still results in below-normal preoperative cranial indices in these patients. In our series, cranial index was universally low preoperatively, and corrected to the normal range at 1-year follow-up. Our pre- and postoperative cranial indices (mean 0.70 and 0.82) were very similar to those reported by Dobbs et al. in their report of single-stage open correction of combined metopic-sagittal synostosis (mean 0.68 preoperatively and 0.80 postoperatively).1

Cranial index was the only anthropometric measurement reported by Dobbs et al., but the stigmata of trigonocephaly in combined metopic-sagittal synostosis also warrant objective evaluation.1 We used 2 previously published measures of trigonocephaly—the ZF-G-ZF angle14,20 and the IFDA,21 a refinement of the previously reported interfrontal angle20 that quantifies the degree of interfrontal narrowing and distinguishes true metopic synostosis from normal variants. Both the ZF-G-ZF angle and IFDA were significantly more acute preoperatively in the study patients relative to normal controls. All 3 study patients measured well below the IFDA threshold of 134° reported by Wood et al.,21 supporting the diagnosis of true metopic synostosis. Postoperatively, both angles were comparable to age-matched normal controls, with a mean ZF-G-ZF angle of 126.6° and a mean IFDA of 139.1°, demonstrating a measurable correction of trigonocephaly and bifrontal narrowing. In endoscope-assisted craniectomy, there is no direct treatment of these deformities intraoperatively, and we instead rely on cranial expansion driven by normal brain growth, with head shape guided by the postoperative molding helmet.14 Our results clearly demonstrate the efficacy of molding helmet therapy in correcting trigonocephaly after adequate and complete suturectomy.

Hypotelorism and deficiency of the superolateral orbital rims are also characteristic of metopic synostosis.26,27 We used the established measurements of intercanthal distance and ZF-ZF distance to assess the degree of these deformities before and after surgery. The mean intercanthal distance was significantly narrower in the study patients than in the controls preoperatively, although the lower end of the normal control range was similar to that of the study patients (Fig. 4). This may reflect either normal variation in intercanthal distance among young infants or inherent limitations of CT-based soft-tissue measurements. Intercanthal distance is known to often be normal in patients with metopic synostosis,28 and may be of limited utility as a diagnostic criterion. Nevertheless, intercanthal distance was comparable between study patients and normal controls postoperatively, and the study patient values were nearer to the median of the normal control range (Fig. 4). We found no significant differences in ZF-ZF distance between patients and controls pre- or postoperatively. Preoperatively, however, 2 study patients had measurements below the range for controls, and all study patient measurements fell within the range of controls postoperatively. An increase in ZF-ZF distance is a key measure showing straightening of the lateral orbital rims (Fig. 5). Although these facial manifestations of metopic synostosis are, again, not directly corrected during endoscope-assisted craniectomy, the complete excision of the fused suture to the level of the nasal upper lateral cartilages (corresponding to the level of the nasofrontal suture in infants;29 see Fig. 1) allows physiological expansion of the craniofacial skeleton driven by normal brain growth.

Helmet design is critical to achieving a normal head shape, and presents a unique challenge in patients with metopic-sagittal synostosis. Whereas a postoperative molding helmet for isolated metopic synostosis repair will have contact with the frontal midline and bilateral temporoparietal regions (allowing lateral frontal and orbital expansion to correct trigonocephaly),14 a helmet for the patient with combined metopic-sagittal synostosis should avoid temporoparietal contact to allow for simultaneous correction of scaphocephaly caused by the sagittal synostosis. The helmet must have good anteroposterior contact while avoiding contact with the lateral forehead, allowing lateral expansion through the temporoparietal and lateral frontal regions. The anterior border of the helmet should fit low on the forehead (at the level of the brow) to prevent inappropriate turricephalic expansion of the vertex. Treatment by an experienced cranial orthotist is preferred, and close communication between surgeon and orthotist is essential to ensure timely identification of any necessary helmet modifications.

Two patients developed postoperative synostosis of the coronal sutures. We have previously reported a 1.7% rate of delayed synostosis of neighboring sutures after endoscopic repairs,30 and this phenomenon has also been documented after open cranial vault remodeling.31 Although the exact pathogenesis is not known, we hypothesize that the higher frequency of postoperative new-onset synostosis in the present series of patients is due to their original presentation with multiple-suture synostosis. They may have a higher predisposition to additional synostoses, whether due to underlying genetic factors or otherwise aberrant development of the cranial sutures. Although neither of our 2 patients with new synostoses had a known syndromic association, we emphasize the importance of genetic evaluation for all patients with multiple-suture craniosynostosis. Nevertheless, at most recent follow-up, the new coronal synostoses did not appear to have a significant impact on head shape or facial development. One patient also developed a sagittal neosuture in the craniectomy site, a pattern well documented after endoscopic repair.32–34 At the 7-year follow-up for the patient in case 1, we also note a mild midfrontal depression (Fig. 6), which we have seen in some patients after endoscopic repair of metopic synostosis. We attribute this to tethering of the frontalis in the plane of dissection for the metopic suturectomy. Subperiosteal dissection in this region may prove useful in avoiding this contour irregularity.

For repairs of both metopic and sagittal synostosis, relapse on long-term follow-up is an additional consideration. Wes et al. reported worsening aesthetic outcomes over time after fronto-orbital advancement for metopic synostosis.35 Studies of relapse after open sagittal synostosis repair have had varied results,22,36–38 and mild long-term regression of cranial index may reflect intentional intraoperative overcorrection. Some degree of regression has also been demonstrated after endoscopic repair of sagittal synostosis, between the conclusion of helmet therapy and several years later.39 In each of our 3 patients, we demonstrated normalization of all 5 anthropometric measures at 1-year follow-up. For the patient in whom a 5-year CT scan was available, each measurement was either stable or improved from the 1-year scan, showing durability of the improvement in head shape over time. This patient did, however, have relapse of an indentation anterior to lambda (Fig. 5), an irregularity not captured in the standard measurements. The cause of this recurrence is unclear, but may be due to an intrinsic growth restriction in the calvarial or dural tissue in this region, given that it was present preoperatively. This pattern was not noted in the patients in cases 2 or 3.

Head circumference curves for all 3 patients demonstrated normal head growth through the postoperative period, during and after helmet therapy. We have previously shown that helmet therapy does not restrict head growth after endoscopic repair of sagittal synostosis,40 and the results in the present study suggest that patients with multiple-suture synostosis can also be safely treated with endoscopic repair and helmet therapy, without calvarial growth restriction.

The endoscopic approach is also likely to afford a significant cost savings relative to open reconstruction. In single-suture metopic and coronal synostoses, we have reported an average savings of $45,000 relative to fronto-orbital advancement, including helmet therapy.17 For multiple-suture synostoses traditionally requiring multiple open operations, a single-stage endoscopic repair could reasonably be expected to impart an even larger cost reduction.

We recognize several limitations to this study including the small sample size, a reflection of the rarity of combined metopic-sagittal synostosis. We were also limited in clinical and radiological follow-up, with 2 patients having only a 1-year postoperative CT scan. Finally, we emphasize that the results obtained with molding helmet therapy are dependent on early surgical intervention to take maximal advantage of skull growth. Our results may not be generalizable to all centers, because we depend on 1) very early referral to meet the ideal age range of 2–3 months for surgery, and 2) collaboration with experienced orthotists for specialized helmet fabrication and adjustments.

Conclusions

Repair of combined metopic-sagittal synostosis by single-stage endoscope-assisted craniectomy and molding helmet therapy corrects the stigmata of trigonoscaphocephaly and normalizes head shape. In patients referred by 2–3 months of age with reliable helmet therapy available, it should be considered a viable alternative to open cranial vault remodeling and fronto-orbital advancement.

Disclosures

Dr. Patel is a consultant for Stryker CMF and an educational speaker for Hanger Clinic. Dr. Naidoo is an educational speaker for Hanger Clinic. Mr. Bellanger is an orthotist for Orthotic & Prosthetic Lab, Inc.

Author Contributions

Conception and design: Patel, Zubovic. Acquisition of data: Zubovic. Analysis and interpretation of data: Zubovic, Skolnick. Drafting the article: Zubovic. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Patel. Statistical analysis: Zubovic, Skolnick. Study supervision: Patel.

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    • Export Citation
  • 9

    Jimenez DF, Barone CM, Cartwright CC, Baker L. Early management of craniosynostosis using endoscopic-assisted strip craniectomies and cranial orthotic molding therapy. Pediatrics. 2002;110(1 Pt 1):97104.

    • Search Google Scholar
    • Export Citation
  • 10

    Jimenez DF, McGinity MJ, Barone CM. Endoscopy-assisted early correction of single-suture metopic craniosynostosis: a 19-year experience. J Neurosurg Pediatr. 2018;23(1):6174.

    • Search Google Scholar
    • Export Citation
  • 11

    Ridgway EB, Berry-Candelario J, Grondin RT, et al. The management of sagittal synostosis using endoscopic suturectomy and postoperative helmet therapy. J Neurosurg Pediatr. 2011;7(6):620626.

    • Search Google Scholar
    • Export Citation
  • 12

    Farber SJ, Nguyen DC, Skolnick GB, et al. Anthropometric outcome measures in patients with metopic craniosynostosis. J Craniofac Surg. 2017;28(3):713716.

    • Search Google Scholar
    • Export Citation
  • 13

    Nguyen DC, Farber SJ, Skolnick GB, et al. One hundred consecutive endoscopic repairs of sagittal craniosynostosis: an evolution in care. J Neurosurg Pediatr. 2017;20(5):410418.

    • Search Google Scholar
    • Export Citation
  • 14

    Nguyen DC, Patel KB, Skolnick GB, et al. Are endoscopic and open treatments of metopic synostosis equivalent in treating trigonocephaly and hypotelorism? J Craniofac Surg. 2015;26(1):129134.

    • Search Google Scholar
    • Export Citation
  • 15

    Seymour-Dempsey K, Baumgartner JE, Teichgraeber JF, et al. Molding helmet therapy in the management of sagittal synostosis. J Craniofac Surg. 2002;13(5):631635.

    • Search Google Scholar
    • Export Citation
  • 16

    Sgouros S, Goldin JH, Hockley AD, et al. Intracranial volume change in childhood. J Neurosurg. 1999;91(4):610616.

  • 17

    Zubovic E, Lapidus JB, Skolnick GB, et al. Cost comparison of surgical management of nonsagittal synostosis: traditional open versus endoscope-assisted techniques [published online January 10, 2020]. J Neurosurg Pediatr. doi:10.3171/2019.11.PEDS19515.

    • Search Google Scholar
    • Export Citation
  • 18

    Daboul A, Schwahn C, Schaffner G, et al. Reproducibility of Frankfort horizontal plane on 3D multi-planar reconstructed MR images [erratum in: PLoS One. 2012;7(11):e48281]. PLoS One. 2012;7(10):e48281.

    • Search Google Scholar
    • Export Citation
  • 19

    Haas LL. Roentgenological skull measurements and their diagnostic applications. Am J Roentgenol Radium Ther Nucl Med. 1952;67(2):197209.

    • Search Google Scholar
    • Export Citation
  • 20

    Kellogg R, Allori AC, Rogers GF, Marcus JR. Interfrontal angle for characterization of trigonocephaly: part 1: development and validation of a tool for diagnosis of metopic synostosis. J Craniofac Surg. 2012;23(3):799804.

    • Search Google Scholar
    • Export Citation
  • 21

    Wood BC, Mendoza CS, Oh AK, et al. What’s in a name? Accurately diagnosing metopic craniosynostosis using a computational approach. Plast Reconstr Surg. 2016;137(1):205213.

    • Search Google Scholar
    • Export Citation
  • 22

    Thomas GP, Johnson D, Byren JC, et al. Long-term morphological outcomes in nonsyndromic sagittal craniosynostosis: a comparison of 2 techniques. J Craniofac Surg. 2015;26(1):1925.

    • Search Google Scholar
    • Export Citation
  • 23

    Jimenez DF, Barone CM. Multiple-suture nonsyndromic craniosynostosis: early and effective management using endoscopic techniques. J Neurosurg Pediatr. 2010;5(3):223231.

    • Search Google Scholar
    • Export Citation
  • 24

    Domeshek LF, Das RR, Van Aalst JA, et al. Influence of metopic suture fusion associated with sagittal synostosis. J Craniofac Surg. 2011;22(1):7783.

    • Search Google Scholar
    • Export Citation
  • 25

    Terner JS, Travieso R, Lee SS, et al. Combined metopic and sagittal craniosynostosis: is it worse than sagittal synostosis alone? Neurosurg Focus. 2011;31(2):E2.

    • Search Google Scholar
    • Export Citation
  • 26

    Delashaw JB, Persing JA, Park TS, Jane JA. Surgical approaches for the correction of metopic synostosis. Neurosurgery. 1986;19(2):228234.

    • Search Google Scholar
    • Export Citation
  • 27

    Ezaldein HH, Metzler P, Persing JA, Steinbacher DM. Three-dimensional orbital dysmorphology in metopic synostosis. J Plast Reconstr Aesthet Surg. 2014;67(7):900905.

    • Search Google Scholar
    • Export Citation
  • 28

    Patel KB, Skolnick GB, Mulliken JB. Anthropometric outcomes following fronto-orbital advancement for metopic synostosis. Plast Reconstr Surg. 2016;137(5):15391547.

    • Search Google Scholar
    • Export Citation
  • 29

    Poublon RM, Verwoerd CD, Verwoerd-Verhoef HL. Anatomy of the upper lateral cartilages in the human newborn. Rhinology. 1990;28(1):4145.

    • Search Google Scholar
    • Export Citation
  • 30

    Yarbrough CK, Smyth MD, Holekamp TF, et al. Delayed synostoses of uninvolved sutures after surgical treatment of nonsyndromic craniosynostosis. J Craniofac Surg. 2014;25(1):119123.

    • Search Google Scholar
    • Export Citation
  • 31

    Seruya M, Tan SY, Wray AC, et al. Total cranial vault remodeling for isolated sagittal synostosis: part I. Postoperative cranial suture patency. Plast Reconstr Surg. 2013;132(4):602e610e.

    • Search Google Scholar
    • Export Citation
  • 32

    Salehi A, Ott K, Skolnick GB, et al. Neosuture formation after endoscope-assisted craniosynostosis repair. J Neurosurg Pediatr. 2016;18(2):196200.

    • Search Google Scholar
    • Export Citation
  • 33

    Shillito J. A new cranial suture appearing in the site of craniectomy for synostosis. Radiology. 1973;107(1):8388.

  • 34

    Sauerhammer TM, Seruya M, Ropper AE, et al. Craniectomy gap patency and neosuture formation following endoscopic suturectomy for unilateral coronal craniosynostosis. Plast Reconstr Surg. 2014;134(1):81e91e.

    • Search Google Scholar
    • Export Citation
  • 35

    Wes AM, Paliga JT, Goldstein JA, et al. An evaluation of complications, revisions, and long-term aesthetic outcomes in nonsyndromic metopic craniosynostosis. Plast Reconstr Surg. 2014;133(6):14531464.

    • Search Google Scholar
    • Export Citation
  • 36

    Fearon JA, McLaughlin EB, Kolar JC. Sagittal craniosynostosis: surgical outcomes and long-term growth. Plast Reconstr Surg. 2006;117(2):532541.

    • Search Google Scholar
    • Export Citation
  • 37

    Agrawal D, Steinbok P, Cochrane DD. Long-term anthropometric outcomes following surgery for isolated sagittal craniosynostosis. J Neurosurg. 2006;105(5)(suppl):357–360.

    • Search Google Scholar
    • Export Citation
  • 38

    van Veelen ML, Eelkman Rooda OH, de Jong T, et al. Results of early surgery for sagittal suture synostosis: long-term follow-up and the occurrence of raised intracranial pressure. Childs Nerv Syst. 2013;29(6):9971005.

    • Search Google Scholar
    • Export Citation
  • 39

    Pickersgill NA, Skolnick GB, Naidoo SD, et al. Regression of cephalic index following endoscopic repair of sagittal synostosis. J Neurosurg Pediatr. 2018;23(1):5460.

    • Search Google Scholar
    • Export Citation
  • 40

    Ghenbot RG, Patel KB, Skolnick GB, et al. Effects of open and endoscopic surgery on skull growth and calvarial vault volumes in sagittal synostosis. J Craniofac Surg. 2015;26(1):161164.

    • Search Google Scholar
    • Export Citation
  • 41

    Shah MN, Kane AA, Petersen JD, et al. Endoscopically assisted versus open repair of sagittal craniosynostosis: the St. Louis Children’s Hospital experience. J Neurosurg Pediatr. 2011;8(2):165170.

    • Search Google Scholar
    • Export Citation

Diagram from Prolo et al. (pp 179–188).

Contributor Notes

Correspondence Kamlesh B. Patel: Washington University in St. Louis, St. Louis, MO. kamlesh.patel@wustl.edu.

INCLUDE WHEN CITING Published online April 17, 2020; DOI: 10.3171/2020.2.PEDS2029.

Disclosures Dr. Patel is a consultant for Stryker CMF and an educational speaker for Hanger Clinic. Dr. Naidoo is an educational speaker for Hanger Clinic. Mr. Bellanger is an orthotist for Orthotic & Prosthetic Lab, Inc.

  • View in gallery

    Intraoperative endoscopic image showing completion of metopic suturectomy with visualization of nasal upper lateral cartilages (ULC). The cranial extent of the upper lateral cartilages indicates the level of the nasofrontal suture in an infant (see Poublon et al.29), confirming complete metopic suturectomy. Figure is available in color online only.

  • View in gallery

    The ZF-G-ZF angle. Angle (red solid line) formed by glabella (solid red circles) and bilateral zygomaticofrontal sutures (open and solid orange circles), projected onto a single axial plane (red dashed line) parallel to the Frankfort horizontal. Originally defined by Kellogg et al.20 and reported in Nguyen et al.14 Figure is available in color online only.

  • View in gallery

    The IFDA as defined by Wood et al.21 On a CT scan oriented to the axial plane containing the opisthion (large yellow circle) and superior-most points of the clinoid processes of the dorsum sellae (small yellow circles), a triangle (orange line) is formed between the anterior-most point of the cranium and the exterior of bilateral coronal sutures. Perpendicular bisectors (orange dashed lines) intersect with the outermost aspect of the frontal bones (red circles). The IFDA (red line) is the angle between these points and the anterior-most point. Figure is available in color online only.

  • View in gallery

    Scatterplots showing anthropometric comparisons; pre- and postoperative values are shown. Study patients with metopic-sagittal synostosis are represented by colored triangles; age-matched controls are represented by open circles. Significant differences between study and control groups are marked with asterisks. Figure is available in color online only.

  • View in gallery

    Chronological CT scans of the 3 study patients, to scale. The patient in case 1 is noted to have a posterior calvarial indentation just anterior to lambda, a deformity previously described after repair of sagittal synostosis (see Shah et al.41). This was present preoperatively, and although it had improved on 1-year postoperative CT scan, it reappeared at 5 years. This irregularity is not noted in the other 2 patients. The patient in case 1 also developed bicoronal synostosis postoperatively. Slight orbital asymmetry and nasal root deviation are noted on 5-year postoperative CT scan. The patient in case 2 developed right unicoronal synostosis, with no notable effect on head shape or facial symmetry at 1 year.

  • View in gallery

    Case 1. Chronological photographs. Helmet therapy was completed at age 12 months. Mild bitemporal retrusion improved over time. A: Preoperative photograph obtained at 5 weeks of age. B: Photograph obtained 5 months postoperatively, at 8 months of age. C: Photograph obtained 1.5 years postoperatively, at 20 months of age. D: Photograph obtained 7 years postoperatively, at 7 years of age. Figure is available in color online only.

  • 1

    Dobbs TD, Salahuddin O, Jayamohan J, et al. The management of trigonoscaphocephaly as a result of combined metopic and sagittal synostosis. Plast Reconstr Surg. 2017;139(6):1325e1332e.

    • Search Google Scholar
    • Export Citation
  • 2

    Greene AK, Mulliken JB, Proctor MR, et al. Phenotypically unusual combined craniosynostoses: presentation and management. Plast Reconstr Surg. 2008;122(3):853862.

    • Search Google Scholar
    • Export Citation
  • 3

    Czerwinski M, Kolar JC, Fearon JA. Complex craniosynostosis. Plast Reconstr Surg. 2011;128(4):955961.

  • 4

    Esparza J, Hinojosa J. Complications in the surgical treatment of craniosynostosis and craniofacial syndromes: apropos of 306 transcranial procedures. Childs Nerv Syst. 2008;24(12):14211430.

    • Search Google Scholar
    • Export Citation
  • 5

    Abbott MM, Rogers GF, Proctor MR, et al. Cost of treating sagittal synostosis in the first year of life. J Craniofac Surg. 2012;23(1):8893.

  • 6

    Han RH, Nguyen DC, Bruck BS, et al. Characterization of complications associated with open and endoscopic craniosynostosis surgery at a single institution. J Neurosurg Pediatr. 2016;17(3):361370.

    • Search Google Scholar
    • Export Citation
  • 7

    Goyal A, Lu VM, Yolcu YU, et al. Endoscopic versus open approach in craniosynostosis repair: a systematic review and meta-analysis of perioperative outcomes. Childs Nerv Syst. 2018;34(9):16271637.

    • Search Google Scholar
    • Export Citation
  • 8

    Lee HQ, Hutson JM, Wray AC, et al. Analysis of morbidity and mortality in surgical management of craniosynostosis. J Craniofac Surg. 2012;23(5):12561261.

    • Search Google Scholar
    • Export Citation
  • 9

    Jimenez DF, Barone CM, Cartwright CC, Baker L. Early management of craniosynostosis using endoscopic-assisted strip craniectomies and cranial orthotic molding therapy. Pediatrics. 2002;110(1 Pt 1):97104.

    • Search Google Scholar
    • Export Citation
  • 10

    Jimenez DF, McGinity MJ, Barone CM. Endoscopy-assisted early correction of single-suture metopic craniosynostosis: a 19-year experience. J Neurosurg Pediatr. 2018;23(1):6174.

    • Search Google Scholar
    • Export Citation
  • 11

    Ridgway EB, Berry-Candelario J, Grondin RT, et al. The management of sagittal synostosis using endoscopic suturectomy and postoperative helmet therapy. J Neurosurg Pediatr. 2011;7(6):620626.

    • Search Google Scholar
    • Export Citation
  • 12

    Farber SJ, Nguyen DC, Skolnick GB, et al. Anthropometric outcome measures in patients with metopic craniosynostosis. J Craniofac Surg. 2017;28(3):713716.

    • Search Google Scholar
    • Export Citation
  • 13

    Nguyen DC, Farber SJ, Skolnick GB, et al. One hundred consecutive endoscopic repairs of sagittal craniosynostosis: an evolution in care. J Neurosurg Pediatr. 2017;20(5):410418.

    • Search Google Scholar
    • Export Citation
  • 14

    Nguyen DC, Patel KB, Skolnick GB, et al. Are endoscopic and open treatments of metopic synostosis equivalent in treating trigonocephaly and hypotelorism? J Craniofac Surg. 2015;26(1):129134.

    • Search Google Scholar
    • Export Citation
  • 15

    Seymour-Dempsey K, Baumgartner JE, Teichgraeber JF, et al. Molding helmet therapy in the management of sagittal synostosis. J Craniofac Surg. 2002;13(5):631635.

    • Search Google Scholar
    • Export Citation
  • 16

    Sgouros S, Goldin JH, Hockley AD, et al. Intracranial volume change in childhood. J Neurosurg. 1999;91(4):610616.

  • 17

    Zubovic E, Lapidus JB, Skolnick GB, et al. Cost comparison of surgical management of nonsagittal synostosis: traditional open versus endoscope-assisted techniques [published online January 10, 2020]. J Neurosurg Pediatr. doi:10.3171/2019.11.PEDS19515.

    • Search Google Scholar
    • Export Citation
  • 18

    Daboul A, Schwahn C, Schaffner G, et al. Reproducibility of Frankfort horizontal plane on 3D multi-planar reconstructed MR images [erratum in: PLoS One. 2012;7(11):e48281]. PLoS One. 2012;7(10):e48281.

    • Search Google Scholar
    • Export Citation
  • 19

    Haas LL. Roentgenological skull measurements and their diagnostic applications. Am J Roentgenol Radium Ther Nucl Med. 1952;67(2):197209.

    • Search Google Scholar
    • Export Citation
  • 20

    Kellogg R, Allori AC, Rogers GF, Marcus JR. Interfrontal angle for characterization of trigonocephaly: part 1: development and validation of a tool for diagnosis of metopic synostosis. J Craniofac Surg. 2012;23(3):799804.

    • Search Google Scholar
    • Export Citation
  • 21

    Wood BC, Mendoza CS, Oh AK, et al. What’s in a name? Accurately diagnosing metopic craniosynostosis using a computational approach. Plast Reconstr Surg. 2016;137(1):205213.

    • Search Google Scholar
    • Export Citation
  • 22

    Thomas GP, Johnson D, Byren JC, et al. Long-term morphological outcomes in nonsyndromic sagittal craniosynostosis: a comparison of 2 techniques. J Craniofac Surg. 2015;26(1):1925.

    • Search Google Scholar
    • Export Citation
  • 23

    Jimenez DF, Barone CM. Multiple-suture nonsyndromic craniosynostosis: early and effective management using endoscopic techniques. J Neurosurg Pediatr. 2010;5(3):223231.

    • Search Google Scholar
    • Export Citation
  • 24

    Domeshek LF, Das RR, Van Aalst JA, et al. Influence of metopic suture fusion associated with sagittal synostosis. J Craniofac Surg. 2011;22(1):7783.

    • Search Google Scholar
    • Export Citation
  • 25

    Terner JS, Travieso R, Lee SS, et al. Combined metopic and sagittal craniosynostosis: is it worse than sagittal synostosis alone? Neurosurg Focus. 2011;31(2):E2.

    • Search Google Scholar
    • Export Citation
  • 26

    Delashaw JB, Persing JA, Park TS, Jane JA. Surgical approaches for the correction of metopic synostosis. Neurosurgery. 1986;19(2):228234.

    • Search Google Scholar
    • Export Citation
  • 27

    Ezaldein HH, Metzler P, Persing JA, Steinbacher DM. Three-dimensional orbital dysmorphology in metopic synostosis. J Plast Reconstr Aesthet Surg. 2014;67(7):900905.

    • Search Google Scholar
    • Export Citation
  • 28

    Patel KB, Skolnick GB, Mulliken JB. Anthropometric outcomes following fronto-orbital advancement for metopic synostosis. Plast Reconstr Surg. 2016;137(5):15391547.

    • Search Google Scholar
    • Export Citation
  • 29

    Poublon RM, Verwoerd CD, Verwoerd-Verhoef HL. Anatomy of the upper lateral cartilages in the human newborn. Rhinology. 1990;28(1):4145.

    • Search Google Scholar
    • Export Citation
  • 30

    Yarbrough CK, Smyth MD, Holekamp TF, et al. Delayed synostoses of uninvolved sutures after surgical treatment of nonsyndromic craniosynostosis. J Craniofac Surg. 2014;25(1):119123.

    • Search Google Scholar
    • Export Citation
  • 31

    Seruya M, Tan SY, Wray AC, et al. Total cranial vault remodeling for isolated sagittal synostosis: part I. Postoperative cranial suture patency. Plast Reconstr Surg. 2013;132(4):602e610e.

    • Search Google Scholar
    • Export Citation
  • 32

    Salehi A, Ott K, Skolnick GB, et al. Neosuture formation after endoscope-assisted craniosynostosis repair. J Neurosurg Pediatr. 2016;18(2):196200.

    • Search Google Scholar
    • Export Citation
  • 33

    Shillito J. A new cranial suture appearing in the site of craniectomy for synostosis. Radiology. 1973;107(1):8388.

  • 34

    Sauerhammer TM, Seruya M, Ropper AE, et al. Craniectomy gap patency and neosuture formation following endoscopic suturectomy for unilateral coronal craniosynostosis. Plast Reconstr Surg. 2014;134(1):81e91e.

    • Search Google Scholar
    • Export Citation
  • 35

    Wes AM, Paliga JT, Goldstein JA, et al. An evaluation of complications, revisions, and long-term aesthetic outcomes in nonsyndromic metopic craniosynostosis. Plast Reconstr Surg. 2014;133(6):14531464.

    • Search Google Scholar
    • Export Citation
  • 36

    Fearon JA, McLaughlin EB, Kolar JC. Sagittal craniosynostosis: surgical outcomes and long-term growth. Plast Reconstr Surg. 2006;117(2):532541.

    • Search Google Scholar
    • Export Citation
  • 37

    Agrawal D, Steinbok P, Cochrane DD. Long-term anthropometric outcomes following surgery for isolated sagittal craniosynostosis. J Neurosurg. 2006;105(5)(suppl):357–360.

    • Search Google Scholar
    • Export Citation
  • 38

    van Veelen ML, Eelkman Rooda OH, de Jong T, et al. Results of early surgery for sagittal suture synostosis: long-term follow-up and the occurrence of raised intracranial pressure. Childs Nerv Syst. 2013;29(6):9971005.

    • Search Google Scholar
    • Export Citation
  • 39

    Pickersgill NA, Skolnick GB, Naidoo SD, et al. Regression of cephalic index following endoscopic repair of sagittal synostosis. J Neurosurg Pediatr. 2018;23(1):5460.

    • Search Google Scholar
    • Export Citation
  • 40

    Ghenbot RG, Patel KB, Skolnick GB, et al. Effects of open and endoscopic surgery on skull growth and calvarial vault volumes in sagittal synostosis. J Craniofac Surg. 2015;26(1):161164.

    • Search Google Scholar
    • Export Citation
  • 41

    Shah MN, Kane AA, Petersen JD, et al. Endoscopically assisted versus open repair of sagittal craniosynostosis: the St. Louis Children’s Hospital experience. J Neurosurg Pediatr. 2011;8(2):165170.

    • Search Google Scholar
    • Export Citation

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