Temporal muscle thickness and area are an independent prognostic factors in patients aged 75 or younger with aneurysmal subarachnoid hemorrhage treated by clipping
- Department of Neurosurgery, Suwa Red Cross Hospital, Suwa, Nagano, Japan.
DOI:10.25259/SNI_814_2020Copyright: © 2021 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Masahito Katsuki, Yukinari Kakizawa, Akihiro Nishikawa, Yasunaga Yamamoto, Toshiya Uchiyama. Temporal muscle thickness and area are an independent prognostic factors in patients aged 75 or younger with aneurysmal subarachnoid hemorrhage treated by clipping. 14-Apr-2021;12:151
How to cite this URL: Masahito Katsuki, Yukinari Kakizawa, Akihiro Nishikawa, Yasunaga Yamamoto, Toshiya Uchiyama. Temporal muscle thickness and area are an independent prognostic factors in patients aged 75 or younger with aneurysmal subarachnoid hemorrhage treated by clipping. 14-Apr-2021;12:151. Available from: https://surgicalneurologyint.com/surgicalint-articles/10719/
Background: Skeletal muscle mass is an important factor for various diseases’ outcomes. As for its indicators, temporal muscle thickness (TMT) and temporal muscle area (TMA) on the head computed tomography are useful, and TMT and TMA were reported as potential prognostic factors for aneurysmal subarachnoid hemorrhage (SAH). We examined the clinical characteristics, including TMT and TMA, of SAH patients aged 75 or younger.
Methods: We retrospectively investigated 127 SAH patients with all World Federation of Neurosurgical Societies (WFNS) grades and treated by clipping between 2009 and 2019. Clinical outcome was measured with the modified Rankin Scale (mRS) at 6 months, with favorable outcome defined as mRS 0–2. The associations between the clinical variables and the outcomes were analyzed.
Results: The mean age was 60.6 (32–74) years, and 65% were women. The mean ± standard deviation of WFNS grade was 2.8 ± 1.4. TMT and TMA were larger in the favorable outcome group than the poor one. Multivariate analysis revealed that age, smoking, WFNS grade, and TMT or TMA were associated with favorable outcome. Receiver operating characteristic analysis found that the threshold of TMT was 4.9 mm in female and 6.7 mm in male, and that of TMA was 193 mm2 in female and 333 mm2 in male.
Conclusion: The odds ratios for TMT and TMA related to clinical outcome were lower than for smoking and WFNS grade; however, on multivariate analysis they remained independent prognostic factors in SAH patients aged 75 or younger treated by clipping. Further studies are needed to confirm these findings.
Keywords: Cerebral aneurysm, Clipping, Prognostic factor, Sarcopenia, Subarachnoid hemorrhage, Temporal muscle thickness and area
Low skeletal muscle mass due to low nutrition or aging (sarcopenia in the broadest sense[
Therefore, we focused on the temporal muscle thickness (TMT), and temporal muscle area (TMA) on the head CT, because TMT and TMA are substituted as useful measures of the total body skeletal muscle mass.[
This study was performed to analyze the clinical characteristics of aneurysmal SAH patients aged 75 or younger who were treated by clipping, with a focus on the temporal muscle. To the best of our knowledge, this is the first study, including the young and middle ages, to examine the relationship between TMT and TMA and outcomes of SAH patients treated by clipping.
We retrospectively retrieved data from medical records of all the 127 aneurysmal SAH patients who were admitted between 2009 and 2019 and treated by clipping at our institution. All the patients included in this study had been independent in their activities in daily livings (ADLs) before the onset of SAH. The diagnosis of SAH was based on the clinical history and the presence of SAH on CT. The hospital’s research ethics committee approved this study, and we gained written informed consent for this study from all of the patients, the legally authorized representative of the patients, or next of kin of the deceased patients. All methods were carried out in accordance with relevant guidelines and regulations (Declaration of Helsinki).
General management of SAH was similar in all cases: all patients were first treated with nicardipine and kept normovolemic with normal blood pressure (systolic blood pressure <140 mmHg). Indication for surgery was established according to the Japanese Guidelines for the Management of Stroke 2009[
All SAH patients who underwent aneurysm clipping received fasudil, cilostazol, and statin as appropriate after the operation. Rehabilitation and nutritional support were started as soon as possible after the operation, and prophylaxis and treatment of complications were also ensured. Intra-arterial infusion of fasudil was performed when necessary for the treatment of symptomatic vasospasm. In addition, a ventriculoperitoneal shunt was performed when hydrocephalus was observed.
We collected data regarding physiological symptoms at admission for patients included in this study, that is, age, sex, WFNS grade, systolic blood pressure, administration of antithrombotic drugs, history of smoking and drinking, hypertension, diabetes mellitus, dyslipidemia, symptomatic vasospasm, ventriculoperitoneal shunt, and postoperative complications (except for symptomatic vasospasm and hydrocephalus). Postoperative complications included infectious diseases, heart failure, rerupture, seizure, and disuse syndrome. We also measured albumin, lymphocyte, triglycerides, total cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein (LDL) cholesterol, glucose, and hemoglobin A1c levels at admission. Albumin, lymphocyte, and total cholesterol are known factors for controlling nutritional status score to assess the nutritional status of the patients.[
We determined the location and size of the aneurysm, Fisher CT scale, TMT, and TMA based on the results of the CT or CT angiography at admission. We used the Aquilion ONE (Canon Medical Systems Corporation, Tochigi, Japan) to take CT and CT angiography images of 0.5 × 0.5 × 1.0 mm voxels. The slice thickness was reconstructed to 5 mm [
Head CT image measuring temporal muscle thickness (TMT) and area (TMA). The slice is 5 mm above the superior wall of the orbit (a). The rectangular part in (a) is enlarged in (b) and (c). CT image representing TMT. The line between the arrows indicates TMT (b). CT image representing TMA (c). Patient with a large TMT and TMA (d); patient with a small TMT and TMA (e).
To evaluate the outcomes, modified Rankin Scale (mRS) scores at 6 months after the operations of all 127 patients were collected by either personal outpatient interviews, reports from the rehabilitation hospital or home doctor, or interviews over the telephone, once the ethical approval was obtained for the study. We dichotomized mRS scores into favorable (mRS 0–2) or poor (mRS 3–6).
Intraclass correlation coefficients were used to test inter-rater reliabilities of TMT and TMA. The associations between TMT and TMA and other factors were investigated by the Mann–Whitney U-test, Fisher’s exact test, or Spearman’s coefficient correlation. R > 0.3 was defined that there was a significant correlation. The results are described as mean ± standard deviation (SD). Associations and outcomes between the clinical variables were analyzed using the Mann–Whitney U-test and Fisher’s exact test. Binomial logistic regression analysis was performed using the preoperative factors with P < 0.05 extracted through the univariate analysis described above. Age and sex were also used for the multivariate analysis to adjust the difference of TMT and TMA related to age or sex. Variables with small sample numbers under 80 were excluded from the multivariate analysis. We also performed receiver operating characteristic (ROC) analysis by sex and analyzed the thresholds of the TMT and TMA related to the outcome. The minimum distance point to (0,1) determined the thresholds. A two-tailed p < 0.050 was considered statistically significant. We conducted this calculation using SPSS software version 24.0.0. (IBM, New York, USA).
Clinical characteristics of the 127 SAH patients (82 women and 45 men) treated by clipping are summarized in [
TMT and TMA and sex, age, laboratory data, or outcome
The intraclass correlation coefficients (2, 2) measuring TMT and TMA were 0.803 and 0.724, respectively. TMT and TMA were significantly larger in men than in women [P < 0.001 for both,
Temporal muscle thickness (TMT) was significantly larger in the favorable outcome groups than in the poor outcome groups (P = 0.001 in both sex, P = 0.007 in female, P = 0.007 in male, respectively) (a). Temporal muscle area (TMA) was also significantly larger in the favorable outcome groups (P = 0.005 in both sex, P = 0.007 in female, P = 0.040 in male, respectively) (b). Receiver operating characteristic (ROC) analysis was performed to determine the threshold of the TMT and TMA for outcomes. The threshold of TMT was 4.9 mm in female (sensitivity = 0.661, specificity = 0.750. AUC = 0.703, 95%CI 0.523–0.811, P = 0.003) and 6.7 mm in male (sensitivity = 0.647, specificity = 0.909. AUC = 0.767, 95%CI 0.602–0.933, P = 0.008) (c). The threshold of TMA was 193 mm2 in female (sensitivity = 0.729, specificity = 0.700. AUC = 0.699, 95%CI 0.536–0.813, P = 0.024) and 333 mm2 in male (sensitivity = 0.735, specificity = 0.727. AUC = 0.699, 95%CI 0.521–0.878, P = 0.049) (d).
Relationship between variables and outcome
Age, WFNS grade, smoking, Fisher group, LDL cholesterol, ventriculoperitoneal shunt, and postoperative complications were also significantly associated with poor outcomes in the univariate analysis (P = 0.014, P < 0.001, P = 0.030, P < 0.001, P = 0.04, P = 0.001, P = 0.016, respectively) [
Threshold of TMT and TMA for outcome
ROC analysis revealed that the threshold of TMT was 4.9 mm in female (sensitivity = 0.661, specificity = 0.750. area under the ROC curve [AUC] = 0.703, 95% CI 0.523–0.811, P = 0.003) and 6.7 mm in male (sensitivity = 0.647, specificity = 0.909. AUC = 0.767, 95%CI 0.602–0.933, P = 0.008) [
Our findings show that TMT and TMA would be ones of the prognostic factors of SAH patients aged 75 or younger treated by clipping, and our study found that the threshold for the outcome of TMT was 4.9 mm in female and 6.7 mm in male, and that of TMA was 193 mm2 in female and 333 mm2 in male.
Skeletal muscle mass and neurosurgical diseases
In addition to our report, several reports on the association between skeletal muscle mass and neurosurgical diseases are reported. Higher skeletal muscle mass reduces the risk of intracranial arterial stenosis and may protect against ischemic stroke.[
These are some speculations of why low skeletal muscle mass is related to the poor prognosis of SAH. Patients with neurosurgical diseases or after surgical treatment are usually bedridden for some time due to impaired consciousness, sedation, or surgical invasion. The skeletal muscle would be further catabolized during such acute treatment and hospitalization, so those with low skeletal muscle mass may have difficulty performing rehabilitation. In addition, low skeletal muscle mass and sarcopenia are related to malnutrition.[
As a potential explanation, the skeletal muscle is an endocrine organ and secretes myokines. One of the myokines, interleukin-6 (IL), is associated with inflammation, and elevated plasma concentrations of IL-6 are seen in patients with lower muscle mass or sarcopenia.[
Usefulness of TMT and TMA as indicators of skeletal muscle mass in neurosurgical diseases
Many studies on the association between skeletal muscle mass and outcomes used psoas muscle cross-sectional area at the level of the third lumbar vertebra,[
Previously, thresholds of TMT in the magnetic resonance imaging (MRI) for the outcomes in various diseases were investigated. TMT in MRI over the median was associated with favorable outcomes in brain metastasis.[
Awareness of the relationship between loss of muscle mass and outcome may lead to new therapeutic targets for patients with unruptured aneurysms before developing SAH. Low skeletal muscle mass is related to malnutrition and aging,[
First, the sample size was small. Second, previous studies reported that sex and age affect temporal muscle mass,[
Furthermore, accurate and standard methods of TMT and TMA measurements were not established. Ranganathan[
TMT and TMA were independent prognostic factors for mRS 6 months after aneurysm clipping in aneurysmal SAH patients 75 years of age or younger of all WFNS grades. Our study found that the threshold for the outcome of TMT was 4.9 mm in female and 6.7 mm in male and that of TMA was 193 mm2 in female and 333 mm2 in male. Further studies are needed to confirm these findings.
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