Hand grip strength as a surrogate marker for postoperative changes in spinopelvic alignment in patients with lumbar spinal stenosis

There are a few studies on the postoperative changes in sagittal alignment and corresponding factors, including hand grip strength (HGS) and muscle performance tests for lumbar spinal stenosis (LSS). Thus, we aimed to determine whether HGS can be a surrogate marker for global sagittal alignment changes after decompression with fusion surgery for LSS. This retrospective observational study included 91 patients who underwent spine fusion surgery for LSS. Radiological spinopelvic parameters, including sagittal vertical axis (SVA), lumbar lordosis (LL), pelvic tilt (PT), pelvic incidence (PI), global tilt (GT), and T1 pelvic angle (T1PA), were analyzed preoperatively and 1 year after posterior decompression and fusion surgery. To assess muscle performance, the 6-m walk (SMT), timed up and go (TUGT), and sit-to-stand (STS) tests were conducted. The relationship between HGS and postoperative SVA was examined through multiple linear regression analysis. Additionally, the relationship between HGS and preoperative/postoperative radiologic spinopelvic parameters and muscle performance test results was analyzed through Pearson's correlation. HGS was significantly correlated with age, preoperative and postoperative SVA, and the muscle performance tests. Furthermore, HGS was a factor that can significantly influence postoperative SVA changes in multiple linear regression analyses. Therefore, HGS may be a good predictor of postoperative SVA change.


Methods
Subjects. This study was approved by our Institutional Review Board and Ethics Committee (Yonsei University Institutional Review Board and Ethics Committee: 2018-2116-001), which issued a waiver regarding the need for informed consent. All experiments were performed in accordance with relevant guidelines and regulations. Between April 2014 and July 2015, 91 patients (43 men, 48 women) with LSS underwent lumbar spine surgery, including posterior decompression and fusion. No patient was diagnosed with hand and wrist-related diseases or cervical spine problems, and all patients were identified for instability or a need for resection > 50% of the facet joints owing to foraminal stenosis and degenerative spondylolisthesis of > grade 2 7,8 . All patients were treated with posterior decompression and posterolateral fusion using local autologous and allo-chip bone grafts and instrumentation. Similarly, other basic demographic data, including age, sex, body mass index (BMI), the existence of osteoporosis, and history of falling, were gathered. The history of falling screening prompted patients or caregivers to write a fall diary each time they visited an outpatient clinic by recording the number of falls in the previous 3 months.
Hand grip strength. Hand grip strength was measured using a JAMAR plus + hand-grip dynamometer (Global Medical Devices, Maharashtra, India). The patients were instructed to squeeze the handle as hard as possible for 3 s, and the maximum contractile force was recorded in kilograms. The tests were performed three times on both hands, and the respective highest values were used in the analysis 9 .
The assessment of physical performance. Radiological measurement and classification into several groups. Standard full-length 36-in. lateral radiographs of the spine were used to assess whole-spine sagittal alignment. The whole-spine lateral radiographs were evaluated before surgery and one year after surgery. The sagittal vertical axis (SVA), thoracic kyphosis (TK), thoracolumbar kyphosis (TLK), lumbar lordosis (LL), pelvic tilt (PT), pelvic incidence (PI), sacral slope (SS), global tilt (GT), pelvic incidence minus lumbar lordosis (PI-LL), and T1 pelvic angle (T1PA) were measured as previously described. SVA was defined as the distance between the C7 plumb line and the posterosuperior corner of the sacrum. Using the Cobb method, LL was measured between the superior endplate of L1 and superior endplate of S1, and TK was measured between the superior endplate of T5 and the inferior endplate of T12. TLK was measured as the angle between the upper endplate of T10 and the lower endplate of L2 11,12 . SS is the angle of the sacral plateau to the horizontal, whereas PT is the angle between a vertical line and the line connecting the center of the femoral head to the center of the sacral plateau of S1. PI is the algebraic sum of the two angles: PT and SS. T1PA was defined as the angle subtended by a line from the femoral head to the center of the T1 vertebral body and a line from the femoral head to the center of the superior sacral endplate. GT was defined as the angle subtended by a line from the center of the superior sacral endplate to the center of the C7 vertebral body and a line from the femoral head to the center of the superior sacral end plate 13,14 . Statistical analysis. Categorical variables were analyzed using the chi-square test, whereas continuous variables were analyzed using Student's t-test to evaluate the differences between the pre-and postoperative measurements. Pearson's correlations between HGS, radiologic parameters, and results of physical performance tests were evaluated. To test the hypothesis that HGS might be independently associated with postoperative SVA, multiple linear regression analyses were performed using an enter method with HGS as the independent variable and postoperative SVA as the dependent variable. Potential confounding factors, such as age, sex, BMI, presence of osteoporosis, history of falling, SMT, TUGT, and STS, were similarly considered independent variables. All statistical analyses were performed using SPSS Statistics 23 (IBM Corp., Chicago, IL, USA). P values < 0.05 were considered statistically significant.

Results
Patient demographics. Ninety-one patients (43 men and 48 women) were enrolled in this study. The mean patient age was 68.0 years (range, 33-86 years). Other demographic descriptions, including sex, BMI, and the existence of osteoporosis, are shown in Table 1.
Pre-and postoperative changes in radiographic/clinical parameters. The pre-and postoperative radiographic/clinical parameters are shown in Table 2. No significant differences were observed in SVA, LL, PT, SS, PI-LL, TK, TLK, GT, and T1PA or history of falling. However, significant differences were observed in TUGT, SMT, and STS, with more improvement in performance at 1-year postoperative follow-up than before surgery.

Discussion
The changes in the sagittal alignment of patients with LSS were investigated after posterior decompression and fusion surgery; additionally, the correlations of HGS with demographic, radiological, and clinical parameters were analyzed, respectively. As sarcopenia is a result of the aging process, HGS was observed to be inversely correlated with age 1,2 . In the initial study design, we focused on the mechanism underlying the improvement of the patient's sagittal alignment as a neurological problem, including the assessment of changes in back pain and claudication after surgery. We hoped that the HGS would be an index of preoperative evaluation because it may affect the muscle performance and radiologic parameters, including LL, TLK, PT, GT, PI-LL, T1PA, after surgery. For the postoperative evaluation, the follow-up period of postoperative clinical outcomes or radiologic parameters could be set to more than two years. However, the period for postoperative follow-up was set as one year because HGS is expected to have a constant value within a year 15,16 . As a diagnostic tool for sarcopenia, we aimed to ascertain the mechanism underlying the effect of HGS on the sagittal alignment and muscle performance in patients with LSS briefly after surgery. Therefore, we did not set the follow-up duration longer to maintain a relatively constant effect for HGS on postoperative clinical outcomes and sagittal alignment.
Moreover, HGS and the postoperative radiologic parameters were observed to be significantly related to and could affect the postoperative global sagittal alignment 17 . Similarly, HGS was associated with postoperative muscle performance and preoperative/postoperative clinical outcomes. Multiple studies, to date, have shown a correlation between clinical outcomes and preoperative HGS after hip fracture, esophageal cancer, and degenerative spinal stenosis surgery, wherein cases with a high HGS demonstrated better surgical outcomes [18][19][20] . These results are similar to those of this study evaluating the correlation between HGS and surgical outcomes in LSS. This study presents similar conclusions regarding clinical outcomes, including muscle performance tests. In this regard, HGS was observed to be a significant influencing factor, and this result suggests that patient-specific HGS is a major influencing factor of postoperative muscle performance. To determine HGS as a predictor of postoperative sagittal alignment, multiple linear analyses were performed. For all covariates except HGS, no statistically significant associations were observed with postoperative SVA. Thus, HGS may be a factor indicating global sagittal alignment that contributes to muscle performance, such as the paraspinal muscles, balancing the global sagittal alignment 3,4,15,21 . A decrease in muscle strength or performance status implies that the sagittal alignment is likely unbalanced in older patients due to the aging process, consistent with the definition of sarcopenia. Supposedly, this study provides useful implications that HGS could serve as a useful predictor of patient outcomes. This study has several limitations. First, it has a retrospective design and was conducted without www.nature.com/scientificreports/ correction or control of the sex ratio. Second, this study has a relatively small sample size and a short follow-up period of 1 year. To better establish the predictive value of HGS for LSS, a prospective study with large sample size and long-term follow-up is necessary to confirm these findings.
conclusion Therefore, these findings suggest that HGS can influence surgical outcomes and postoperative sagittal radiologic parameters in patients with LSS and that preoperative HGS may be a good predictor of postoperative SVA status.