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Sci Rep
Sci Rep
Scientific Reports
2045-2322
Nature Publishing Group UK London

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10.1038/s41598-024-71185-w
Article
Upright CT-based evaluation of the effects of posture on skull-base reconstruction after endoscopic endonasal surgery
Takahara Kento 1
Mizutani Katsuhiro katsu512@yahoo.co.jp

1
Yamada Yoshitake 2
Yamada Minoru 2
Yokoyama Yoichi 2
Yoshida Keisuke 1
Kosugi Kenzo 1
Ueda Ryo 1
Toda Masahiro 1
Jinzaki Masahiro 2
1 https://ror.org/02kn6nx58 grid.26091.3c 0000 0004 1936 9959 Department of Neurosurgery, Keio University School of Medicine, Tokyo, Japan
2 https://ror.org/02kn6nx58 grid.26091.3c 0000 0004 1936 9959 Department of Radiology, Keio University School of Medicine, Tokyo, Japan
1 9 2024
1 9 2024
2024
14 203037 4 2024
26 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Cerebrospinal fluid (CSF) leakage is a common complication associated with endoscopic endonasal skull-base surgery (EESBS). Postoperative mobilization-associated postural changes are considered to cause CSF leakage. However, no study has demonstrated a robust relationship between postural changes and CSF leakage. We used upright computed tomography (CT) to clarify the effects of postural changes on the reconstructed skull base (RSB) after EESBS. Thirty patients who underwent EESBS at our institution were prospectively included, and their upright and supine CTs were compared to measure morphological changes in the RSB. Patient clinical data were also collected from medical charts and surgical videos, and their relationships with morphological changes were assessed. In upright CTs, the RSB shifted intracranially by 0.94 (0.0–2.9) mm on average. This shift was larger in cases with lesions extending to the sphenoid sinus, dural defects, intraoperative pulsation of the RSB, and large bone windows. The direction of the change was opposite to intuitive movement driven by gravity because of reduced intracranial pressure in the sitting position. Thus, these shifts can be directly associated with postoperative CSF leakage caused by reconstruction material displacement. Skull-base reconstruction and postoperative postural management accounting for these morphological changes may be necessary for preventing CSF leakage.

Keywords

CSF leakage
Endoscopic endonasal skull-base surgery
Postural changes
Reconstructed skull base
Subject terms

Neuroscience
Brain
Japan Society for the Promotion of Science (JSPS) KAKENHIJP23K07214 JP21H03799 JP20K08056 issue-copyright-statement© Springer Nature Limited 2024
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pmcIntroduction

Cerebrospinal fluid (CSF) leakage is one of the most severe complications of endoscopic endonasal skull-base surgery (EESBS). The postoperative mobilization accompanying postural changes is considered a major cause of CSF leakage. Consequently, most experts recommend bed rest for high-risk patients, such as those with large skull-base defects1,2. Although no reports have shown a robust relationship between postural changes and CSF leakage, to our knowledge, neurosurgeons empirically force patients into postoperative long-term bed rest in daily clinical situations. Furthermore, the effects of postural changes on the reconstructed skull base (RSB) after EESBS have not yet been investigated radiologically.

The recent development in upright computed tomography (CT) scan has helped objectively evaluate posture-related changes in the body, including the brain, with high-quality images comparable to those of a conventional supine CT scan3–5. The intuitive movement of RSB is the shift to the intranasal side in the upright posture, while reduced intracranial pressure (ICP) in the upright posture can drive the opposite force6. We hypothesized that postoperative postural changes cause morphological changes on RSB driven by gravity or changed ICP that can lead to postoperative CSF leakage.

In the present study, we used upright CT scans to clarify how postural changes affect the RSB after EESBS and discussed the mechanisms underlying CSF leakage and optimal perioperative management.

Methods

This prospective, single-arm, exploratory, interventional study was approved by the Ethics Committee of Keio University School of Medicine (approval number: 20180036). This study was conducted in accordance with the guidelines of the Declaration of Helsinki for investigations involving human subjects.

Study population

The present study prospectively included 33 patients aged ≥ 20 years who underwent EESBS at our institution between April 2019 and December 2022 and provided informed consent. All included patients were independent and able to walk. The patients underwent both upright and conventional supine CT scans on the same day during postoperative hospitalization (1–2 weeks after the operation). Patients whose RSB could not be identified on CT owing to intranasal packing or other conditions were excluded from the study.

Surgical procedure

The bi-nostril approach was used for EESBS at our institution. We performed graded skull-base reconstructions based on intraoperative CSF leakage and dural defects. For cases with no intraoperative CSF leakage, oxidized cellulose or abdominal fat was used. Sphenoid sinus mucosa was also used if it was available. For Esposito’s grades 1 or 2 leakage7, abdominal fat combined with nasoseptal flap coverage was performed. For Esposito’s grade 3 leakage, multilayered reconstruction using abdominal fat, fascia, and a nasoseptal flap was performed. In recent cases with Esposito’s grade 3 leakage in the anterior skull base, closure using fascia sutured at its anterior side and a nasoseptal flap was performed. In each case, the reconstruction was performed considering the amount of intraoperative CSF leakage and reported risk factors8–11. Rigid reconstruction was not performed at our institution.

Image acquisition

The patients underwent an upright CT scan (prototype TSX-401R; Canon Medical Systems, Otawara, Japan) in the sitting position (Fig. 1) (An informed consent was obtained from the person in Fig. 1 for publication of identifying images in an online open-access publication) and a conventional supine CT scan (Aquilion ONE; Canon Medical Systems) in the supine position in a prospectively randomized order. The upright CT scan was performed with 320 detector rows, and its performance was comparable to that of a conventional supine CT scan, as described previously3,12–14. Both CT scans were performed under the same conditions at 120 kVp, with a noise index of 4 for a 5-mm slice thickness. CT images with a cross-sectional thickness of 0.5 mm and a cross-section of 0.5 mm were obtained. Image reconstruction was performed using Adaptive Iterative Dose Reduction 3D (Canon Medical Systems), which reduces the radiation dose15.Fig. 1 The upright CT scan in which the patient was placed in the seated position. An informed consent was obtained from the person in this figure for publication of identifying images in an online open-access publication. CT computed tomography.

Image analysis

CT images were analyzed using three-dimensional image analysis software (Synapse Vincent version 5.3; FUJIFILM Medical Co., Ltd., Lexington, MA, USA). First, we fused the upright and supine CT images on the basis of the skull bone. Second, we qualitatively assessed the morphological changes in the RSB in each case as follows: the vertical positional shift of the RSB was measured along a perpendicular bisector axis connecting both bone-deficit ends on a median sagittal plane (Fig. 2). All of the measurements were checked by two neurosurgeons. The CT scans in both positions were evaluated without position labels, and the RSB values were measured by one neurosurgeon and verified by another. Large discrepancies among the observers were resolved through discussions.Fig. 2 Median saggital plane of CT image of a case showing axis along which the RSB shift was measured (A), width of the bone window (B), and thickness of the RSB (C). CT computed tomography, RSB reconstructed skull base.

The association of the following surgical factors with a vertical shift of the RSB was assessed: width of the bone window (measured as the distance between both ends on a median sagittal plane), thickness of the RSB (measured as the distance between the measurement point of the shift of the RSB and the nearest CSF on a median sagittal plane of the upright CT image) (Fig. 2), and the width-to-thickness ratio of the RSB, which was defined as (width of the bone window) / (thickness of the RSB) for quantifying features.

Clinical data collection

Clinical data were collected from medical charts to assess their relationship with shifts in the RSB. The following data were collected: age, sex, height, weight, body mass index, pathology, lesion localization (suprasellar extension or extension to the sphenoid sinus), extent of removal during the operation, intraoperative CSF leakage, reconstruction method, and postoperative CSF leakage. The following data were collected from the operation video recordings: dural defect after manipulation of the lesion and pulsation of the RSB (none, pulsation is not detectable; minor, pulsation is detectable but not detectable as continuous movement of the skull base; and major, pulsation is detectable as continuous movement of the skull base).

Statistical analysis

Statistical analyses were performed using GraphPad Prism 8 software (GraphPad Software, San Diego, CA, USA). The amount of shift of RSB scores was expressed as means with standard deviations and compared using Student’s t-test for non-continuous variables. Correlations between the numerical parameters were assessed using Pearson’s correlation test. Statistical significance was set at P < 0.05.

Results

In total, 30 patients (14 men and 16 women; mean age: 54.4 ± 18.4 years) were included. Three patients were excluded because RSB could not be identified in CT images. The patients underwent surgeries for the following pathologies: nonfunctional pituitary neuroendocrine tumor (PitNET), n = 20; chordoma, n = 3; Rathke’s cleft cyst, n = 2; meningioma, n = 2; craniopharyngioma, n = 1; spontaneous CSF leakage (clivus), n = 1; and sellar arachnoid cyst, n = 1. A lumbar drain was inserted in one case of chordoma. The materials used for skull-base reconstructions were as follows: a nasoseptal flap was used in 14 cases (46.7%), abdominal fat was used in 14 cases (46.7%), abdominal fascia was used in 8 cases (26.7%), and fascial suturing was performed in 5 cases (16.7%). Postoperative CSF leakage was observed in one patient with a nonfunctional PitNET and was surgically repaired.

Most cases showed a shift of the RSB on the fused image of the upright and supine CT scans (Fig. 3A,B). In all observed shifts, the RSB shifted intracranially in the upright CT scan. This inward shift of RSB (ISRSB) was 0.94 mm on average (0.0–2.9 mm) (Fig. 3C). In the case with CSF leakage, ISRSB was 1.7 mm and larger than average. In this case, a CT scan was obtained 10 days after surgery, and the CSF was observed 12 days after surgery.Fig. 3 Fused image of the median sagittal plane of the upright and supine CTs in patients with (A) craniopharyngioma and (B) sellar arachnoid cyst. The surface of the RSB in the upright and supine CT is shown with yellow and red dotted line, respectively. (C) ISRSB with the measuring point in the supine CT set as zero. CT computed tomography, RSB reconstructed skull base, ISRSB inward shift of reconstructed skull base.

ISRSB was larger in cases with lesions extending to the sphenoid sinus (1.70 ± 0.83 mm vs. 0.65 ± 0.56 mm, p = 0.0004; Table 1). ISRSB was also larger in cases with a dural defect after manipulation of the lesion (1.24 ± 0.62 mm vs. 0.58 ± 0.37 mm, p = 0.0189; Table 1). All patients with lesions extending to the sphenoid sinus showed a larger dural defect after manipulation of the lesion; therefore, these two conditions overlapped considerably. Pulsation of the RSB was related to ISRSB; cases showing major pulsation showed larger ISRSB than those with no pulsation (1.23 ± 0.75 mm vs. 0.42 ± 0.42 mm, p = 0.0452). ISRSB value in the minor pulsation group was between those in the no and major pulsation groups (Fig. 4A). The width of the bone window showed a positive correlation with ISRSB (r = 0.4085, p = 0.0250; Supplementary Fig. 1A). Furthermore, the width-to-thickness ratio of the RSB showed a stronger correlation with ISRSB (r = 0.7109, p < 0.0001; Fig. 4B), while thickness of RSB was not significantly correlated with ISRSB (p = 0.2288).Table 1 The relation between clinical features and the ISRSB.

	Number	ISRSB (mm, mean ± SD)	p value	
Patient characteristics	
Age	
 55	15	0.87 ± 0.89	0.6663	
 < 55	15	0.99 ± 0.68	
Sex	
 Male	14	1.11 ± 0.91	0.2545	
 Female	16	0.78 ± 0.64	
BMI	
 ≧ 25	15	1.15 ± 0.88	0.1328	
 < 25	15	0.71 ± 0.62	
Pathology	
 Pit NET	20	0.86 ± 0.70	0.4689	
 Non-Pit NET	10	1.08 ± 0.96	
Preoperative image	
Sphenoid sinus invasion	
 +	8	1.70 ± 0.83	0.0004	
 −	22	0.65 ± 0.56	
 Suprasellar extension	
  +	23	0.80 ± 0.62	0.0893	
  −	7	1.37 ± 1.12	
Intraoperative findings	
 Intraoperative CSF leakage	
  +	13	1.01 ± 0.89	0.6436	
  −	17	0.87 ± 0.72	
 Extent of removal	
  GTR or NTR	14	0.79 ± 0.81	0.3385	
  STR or PR	12	1.12 ± 0.88	
 Dural defect	
  +	16	1.24 ± 0.85	0.0189	
  −	14	0.58 ± 0.54	
Materials used in reconstruction	
 Fat graft	
  +	14	0.94 ± 0.77	0.9348	
  −	16	0.92 ± 0.82	
 Nasoseptal flap	
  +	14	1.01 ± 0.85	0.6231	
  −	16	0.86 ± 0.74	
Significant values are in bold.

ISRSB inward shift of reconstructed skull base, BMI body mass index, CSF cerebrospinal fluid, GTR gross total removal, NTR nearly total removal, STR subtotal removal, PR partial removal.

Fig. 4 (A) Relation between pulsation of the RSB and ISRSB. (B) Correlation between width-to-thickness ratio and the ISRSB. *p < 0.05. RSB reconstructed skull base, ISRSB inward shift of reconstructed skull base.

Discussion

In this study, the effect of postural changes on the RSB was radiologically visualized using upright CT scans. When patients changed their posture from the supine to the sitting position, the RSB shifted intracranially, which was opposite to intuitive movement driven by gravity. Similar findings have not been previously described in the literature.

ISRSB in the sitting position appeared to be driven by changes in the ICP. The ICP is known to decrease in the sitting position compared with that in the supine position6, whereas intranasal pressure is almost equal to atmospheric pressure and is not affected by postural changes. The transition from the supine to the sitting position leads to a relatively negative ICP, driving ISRSB.

Among clinical features, lesions extending to the sphenoid sinus and postoperative dural defects were significantly associated with a larger ISRSB. Furthermore, ISRSB was significantly larger in cases with large bone windows and a large width-to-thickness ratio of the RSB. The bony and dural tissues are the natural boundaries between the extracranial and intracranial spaces. Large defects in these tissues directly expose a larger area to the outer pressure, leading to larger ISRSB, whereas narrow deficits resist the difference between the inner and outer pressures. In the present study, RSB pulsation was also positively associated with ISRSB (Fig. 4A), which is driven by ICP changes caused by pulsatile cardiac output16. Pulsation of the RSB serves as an indicator of its susceptibility to even minor fluctuations in ICP, highlighting its sensitivity to changes in intracranial dynamics.

We assumed that ISRSB are directly associated with postoperative CSF leakage. Shifts in the RSB may lead to the displacement of reconstruction materials from the attached sites, creating the CSF discharge route. Indeed, the case showing CSF leakage in our study showed a relatively large ISRSB compared with the average value. In addition, previous studies have reported that major dural defects are risk factors for postoperative CSF leakage8,9, which is consistent with our findings, since a larger dural defect was directly associated with ISRSB. While postoperative CSF leakage is a severe complication of EESBS, the direct cause of postoperative CSF leakage remains to be elucidated, although several hypotheses have been proposed, including reconstruction site movement induced by CSF pressure and/or CSF pulsation11,17–19. In the absence of studies reporting direct observation of the reconstruction site during postural changes, the influence of postural changes on reconstruction remains uninvestigated. Nevertheless, advances in imaging techniques using sitting CT scans can facilitate direct evaluation of the influence of physical orientation, leading to the assumptions mentioned in the first sentence of this section.

The literature describes many strategies, including the use of a lumbar drain, rigid reconstruction, dural suturing, and multilayered reconstruction to prevent postoperative CSF leakage9,17,20–23. Based on the findings of the present study, we believe that reconstruction should be performed while taking ISRSB into account. A sufficient margin of reconstruction material is necessary to appropriately cover the skull-base defect when ISRSB occurs. Considering ISRSB in the upright position, onlay materials may be indispensable, even if sufficient reconstruction without it seems possible during surgery in the supine position. To make the RSB resistant to the shift, rigid reconstruction or dural suturing may be beneficial. Since a lower width-to-thickness ratio is important for minimizing ISRSB, multilayered reconstruction should be considered for cases with large bony/dural defects, which was reported to be effective24. Intraoperative pulsation of the RSB indicates that the RSB has already been affected by CSF pressure fluctuations and that the patients have a higher risk of CSF leakage. Therefore, an additional robust reconstruction should be considered.

The current study also suggests that postoperative management that minimizes the shift in the RSB is beneficial in preventing CSF leakage. According to the literature6, the ICP was 9.4 ± 3.8 mmHg in the supine position, 4.8 ± 3.6 mmHg in the 10° head-up tilt, 1.3 ± 3.6 mmHg in the 20° head-up tilt, and − 2.4 ± 4.2 mmHg in the standing position. The ICP change was maximal (11.8 mmHg) when the patient changed from the supine to the standing position, while it was much lower (3.7 mmHg) if the patient’s posture changed from the 20° head-up tilt to the standing position. Thus, maintaining the head-up tilt rather than the supine flat position may be feasible and effective in minimizing shifts in the RSB. This position is also beneficial for reducing the constant CSF pressure inside the RSB25. The discussion here supports the recommendation of Fowler’s position rather than the flat supine position in previous studies1,25.

This study had several limitations. First, owing to the small number of cases showing CSF leakage, the relationship between the shift in RSB and postoperative CSF leakage could not be shown directly. Second, we did not perform a rigid reconstruction for EESBS. Rigid reconstruction may be beneficial for reducing shifts in the RSB; however, this was not evaluated in the present study. Third, the ICP was not measured in this study. Patients with EESBS ICP may differ from those reported in other studies. Fourth, CT findings are not always consistent with the real RSB anatomy.

Conclusions

Morphological changes in RSB caused by postural changes were visualized in this study. A cranial shift of the RSB is a common postoperative finding. We assumed that this shift may directly lead to CSF leakage after EESBS. Skull-base reconstruction and postoperative postural management accounting for these morphological changes may be important in preventing CSF leakage.

Supplementary Information

Supplementary Legends.

Supplementary Figure 1.

Supplementary Information

The online version contains supplementary material available at 10.1038/s41598-024-71185-w.

Acknowledgements

We would like to thank Editage (www.editage.jp) for English language editing.

Author contributions

Conceptualization, K.T. and K.M.; investigation, K.T., K.M., Y.Y., M.Y.,and Y.Y.; writing—original draft reparation, K.T.; writing—review and editing, K.M., Y.Y., M.Y.,Y.Y., and M.J.; supervision, K.M. and M.J. All authors haveread and agreed to the published version of the manuscript.

Funding

This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI (Grant Numbers JP23K07214, JP21H03799, and JP20K08056) and Takeda Science Foundation. The authors thank Naomi Tamaki, Yoko Tauchi, and Kyoko Komatsu for their valuable assistance.

Data availability

The datasets generated during the current study are available from the corresponding author on reasonable request.

Competing interests

Masahiro Jinzaki received a grant from Canon Medical Systems, which loaned the upright CT device to Keio University. The funder was not involved in the design of the study; collection, analysis, and interpretation of the data; or writing of the manuscript. The other authors declare that they have no conflict of interest.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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