The effect of sarcopenia in the clinical outcomes following stand-alone lateral lumbar interbody fusion

Abstract

BACKGROUND:

Sarcopenia has been found to affect the postoperative outcomes of lumbar surgery. The effect of sarcopenia on the clinical outcomes in patients who underwent stand-alone lateral lumbar interbody fusion (LLIF) has not yet been examined.

OBJECTIVE:

To investigate whether sarcopenia affects the Oswestry Disability Index (ODI) and visual analog scale (VAS) score for back pain following single-level stand-alone LLIF.

METHODS:

Patients who underwent a single level stand-alone LLIF for lumbar diseases were retrospectively investigated. Sarcopenia was defined according to the diagnostic algorithm recommended by the Asian Working Group for Sarcopenia. Patients were divided into the sarcopenia (SP) and non-sarcopenia (NSP) group. Univariate analysis was used to compare with regards to demographics and clinical outcomes. Multivariate logistic regression was performed to elucidate factors predicting poor clinically improvement.

RESULTS:

Sixty-nine patients were enrolled, with 16 and 53 patients in the SP and NSP group respectively. In the SP group, patients were much older ( $P=$ 0.002), their body mass index was significantly lower ( $P<$ 0.001), the percent of women was higher ( $P=$ 0.042), and the skeletal muscle mass index (SMI) ( $P<$ 0.001) and gait speed were much lower ( $P=$ 0.005). The postoperative ODI scores were much higher and the improvement rate was much lower (both $P<$ 0.001) in the SP group, whereas VAS scores for back pain showed no difference between the two groups. SMI and gait speed had a moderate and weak correlation with the final ODI score, respectively. Low SMI and low gait speed were independently associated with poor clinical outcomes at the final follow-up.

CONCLUSIONS:

Sarcopenia impacts the final clinical outcomes of stand-alone LLIF for lumbar diseases. Low SMI and low gait speed were negative impact factors for the clinical improvement after stand-alone LLIF.

Keywords

Sarcopenia lateral lumbar interbody fusion stand-alone outcome

1. Introduction

Chronic low back pain is one of the most common sources of disability and currently represents a significant burden on healthcare resources [1, 2]. With the aging of the population, its incidence rate is increasing. Lumbar fusion is designed to alleviate pain by inhibiting the motion at the level thought to be responsible for the pain [3, 4]. Lateral lumbar interbody fusion (LLIF) is a minimally-invasive alternative to the traditional anterior and posterior approach, which can achieve nerve decompression indirectly, without posterior incisions or destroying posterior elements [5]. Many reports have evidenced that stand-alone LLIF can effectively relieve symptoms and improve quality of life for the treated patients [6, 7].

In recent years, there has been an increase in research studying the influence of factors on the clinical outcomes following lumbar fusion surgery and many preoperative factors have been shown to influence the postoperative clinical outcomes following lumbar fusion surgeries. For example, age [8], body mass index (BMI) [9], comorbidities [10], and preoperative pain and function [11] have been identified to be associated with the postoperative outcomes following lumbar fusion.

Sarcopenia is defined as a syndrome characterized by progressive loss of skeletal muscle mass and function with resultant disability [12, 13]. Sarcopenia may be a sign of malnutrition, physical disability and immobility, increased frailty and poor quality of life, which can have a significant impact on the health and functional status in older people [12]. In recent years, many studies have demonstrated that there was a correlation between sarcopenia and the clinical outcomes in patients following lumbar surgery [14, 15, 16].

To the best of our knowledge, no study has yet evaluated the relationship between sarcopenia and clinical outcomes in patients who underwent stand-alone LLIF. Therefore, the aim of this study was to determine the effects of sarcopenia on the clinical outcomes in patients undergoing single level stand-alone LLIF for lumbar diseases. We hypothesized that sarcopenia may adversely affect the clinical outcome following stand-alone LLIF.

2. Methods

2.1 Participants

This study was approved by the ethics review boards of Second Affiliated Hospital, School of Medicine, Zhejiang University. All patients signed a written informed consent form and this study was performed in accordance with the Declaration of Helsinki. Between June 2016 and April 2019, patients with degenerative lumbar disease who were treated with stand-alone LLIF at L3-4 or L4-5 levels were considered for this study. All included patients had failed conservative treatment for 6 months.

Inclusion criteria were 1) patients who underwent stand-alone LLIF for lumbar spinal stenosis, degenerative spondylolisthesis, spondylolytic spondylolisthesis, and discogenic low back pain; 2) at least 12 months of follow-up. Exclusion criteria were 1) patients with current major depression, or history of alcohol abuse; 2) patients with diseases affecting the skeletal muscle function; 3) lacking a preoperative lumbar MRI, incomplete pre- or post-operative patient-reported outcomes scores; 4) severe osteoporosis; and 5) previous lumbar fracture and surgery [17, 18, 19].

2.2 Preoperative sarcopenia assessment

Sarcopenia was defined according to the recommended diagnostic algorithm of the Asia Working Group for Sarcopenia (AWGS) [20]. First, muscle mass were assessed by Inbody 770 (Inbody Co., Ltd, Seoul, Korea). Skeletal muscle mass index (SMI) was defined by dividing appendicular skeletal muscle mass by height in meters squared. Handgrip strengths of the dominant hand were measured using a standard adjustable digital handgrip dynamometer Camry EH101 (Guangdong Xiangshan Co., LTD, China). Every patient’s usual walking speed (m/s) on a 6-m course was used as an objective measure of physical performance. Each patient underwent three tests and the tests were performed at a time interval of 90 min to minimize the effect of fatigue on the measurements. The best performance was included in the final analysis.

Using the cut-off points from the AWGS consensus [20], low SMI was defined as $<$ 7.0 kg/m ${}^{2}$ for men and $<$ 5.7 kg/m ${}^{2}$ for women; low hand grip strength was defined as $<$ 26 kg for men and $<$ 18 kg for women; and slow gait speed was defined as $<$ 0.8 m/s. Sarcopenia was defined as low SMI plus low handgrip strength or low walking speed. Patients were allocated to the sarcopenia (SP) or non-sarcopenia (NSP) group based on individual measurement.

2.3 Surgical procedure

LLIF was performed as we previously reported [21]. In short, LLIF was performed under direct visualization and intraoperative electromyographic monitoring. The patient was placed in the lateral decubitus position and slight table flexion was used to increase the space between the ribs and pelvis, which also tensioned the lateral soft tissues. A single transverse or oblique incision about 4 cm targeted to the center of the desired intervertebral space was made. Then the three abdominal layers were split and psoas muscle was split longitudinally along the muscle fiber. Complete discectomy was performed with different dilators gradually expanding at multiple angles. The contracture annulus fibrosus was bluntly released. A large rectangular polyetheretherketone cage (Shanghai Sanyou Medical Co., Ltd, China) packed with allograft demineralized bone matrix mixed with bone marrow aspirate. When the cages were inserted, special care was taken to span the apophyseal rings of endplates. All patients wore the back brace for 3 months postoperatively.

2.4 Clinical outcomes measurements

Pre-operative and final patient-reported outcomes scores, including the Oswestry Disability Index (ODI) and back pain VAS scores, were included for analysis. Poor clinically improvement was defined as improvement $<$ 40% for ODI [22]. Demographic data, including age, gender, body mass index (BMI), bone mineral density (BMD), smoking status, comorbidity, surgical levels and surgical time were also recorded.

2.5 Statistical analysis

Data analysis was performed using SPSS software (Version 19.0 IBM Armonk, NY). Continuous variables were tested with the Kolmogorov-Smirnov test for normal distribution and the Levene test for homogeneity of group variances. Data were expressed as means $\pm$ standard deviation for normally distributed variables, and medians and interquartile intervals for non-parametric data. Unpaired $t$ -test was used to analyze was performed for the analysis of the difference when the data met the assumptions of normality and homogeneity, otherwise the Mann-Whitney U test was used. Categorical variables were measured as frequency or percentage and Chi-square test was used to determine any significant difference. Pearson’s correlation coefficient and simple regression analysis were used for analyzing the correlations between variables. The correlation was classified as very strong ( $\geqslant$ 0.80), strong (0.60–0.79), moderate (0.40–0.59), weak (0.20–0.39), or very weak [23]. Multivariate logistic regression was performed to elucidate factors (age, gender, preoperative ODI and VAS scores, low SMI, low handgrip strength and low walking speed) predicting poor clinical outcomes. Statistical significance was determined at the $P<$ 0.05 level, shown with 95% confidence intervals (CI) throughout.

Figure 1.

Pie chart of the incidence of sarcopenia in the enrolled patients.

3. Results

Sixty-nine patients who met the inclusion criteria and the related medical records were reviewed. There were 28 (40.6%) men and 41 (59.4%) women, with an average age of 62.7 years old. Preoperative diagnoses were degenerative lumbar spinal stenosis in 11 (15.9%) patients, degenerative spondylolisthesis in 32 (46.4%) patients, spondylolytic spondylolisthesis in 21 (30.4%) patients, and discogenic low back pain in 5 (7.2%) patients. Surgical level was L3-4 in 13 (18.8%) patients, while L4-5 in 56 (81.2%) patients. The median duration of was 48.0, whereas the mean follow-up period was16.3 $\pm$ 2.1 months.

There were 16 (23.2%), 4 (5.8%), 16 (23.2%), 16 (23.2%), 2 (2.9) and 15 (21.7%) patients diagnosed as sarcopenia, low SMI, low hand scrip strength, low gait speed, low hand scrip strength plus low gait speed and normal, respectively (Fig. 1). Table 1 showed the comparison result of demographics data of patients from SP and NSP group. There were 3 men and 13 women in the SP group, whereas there were 25 men and 28 women in the NSP group. The patients in the SP group were much older ( $P=$ 0.002) and the BMI was significantly lower than those of the NSS group ( $P<$ 0.001). The percent of women in the SP group was 81.3% (13/16), which was much higher (52.8%, 28/53) than that in the NSS group ( $P=$ 0.042). However, there was no significant difference in BMD, smoking status, duration of symptoms, diagnosis, operative time, surgical levels, and comorbidity between the two groups.

Table 1
Demographic data of the recruited patients

	SP group (No. $=$ 16)	NSP group (No. $=$ 53)	$P$	$Z/\chi 2/t$ score
Age [year, $M(P_{25},P_{75})$ ]	66.5 (59.3, 75.8)	59.0 (56.0, 64.0)	0.002	$-$ 3.028 ${}^{*}$
Gender (M/F)	3/13	25/28	0.042	4.177 ${}^{\S}$
BMI (kg/m ${}^{2}$ )	19.9 $\pm$ 2.9	24.3 $\pm$ 4.4	$<$ 0.001	$-$ 3.722 ${}^{\#}$
BMD [T score, $M(P_{25},P_{75})$ ]	$-$ 2.1 ( $-$ 2.4, $-$ 1.8)	$-$ 2.2 ( $-$ 2.0, $-$ 1.8)	0.542	$-$ 0.608 ${}^{*}$
Smoking (Y/N)	3/13	9/44	0.870	0.027 ${}^{\S}$
Duration of symptoms [month, $M(P_{25},P_{75})$ ]	51.0 (39.0, 72.0)	48.0 (30.0, 71.0)	0.258	$-$ 1.132 ${}^{*}$
Operative time (min)	67.7 $\pm$ 24.3	78.3 $\pm$ 23.6	0.109	$-$ 1.624 ${}^{{\#}}$
Diagnosis (No.)
Lumbar spinal stenosis	3	8	0.642	1.676 ${}^{\S}$
Spondylolytic spondylolisthesis	5	16
Degenerative spondylolisthesis	8	24
Lumbar discogenic pain	0	5
Surgical level (No.)			0.459	0.546 ${}^{\S}$
L3-4	2	11
L4-5	14	42
Comorbidity (No.)
Hypertension	3	8	0.807	1.612 ${}^{\S}$
Diabetes	2	4
COPD	0	4
Osteoarthritis	1	3
Other diseases	1	3

SP: sarcopenia; NSP: non-sarcopenia; M: male; F: female; BMI: body mass index, BMD: bone mineral density; Y/N: yes/no; COPD: chronic obstructive pulmonary disease. ${}^{*}$ : Z score; ${}^{\S}$ : $\chi^{2}$ score; #: t score.

Table 2

Comparison of indexes of sarcopenia and patient-reported outcome scores

	SP group (No. $=$ 16)	NSP group (No. $=$ 53)	$P$ value	$t/Z$ score
SMI [kg/m ${}^{2}$ , $M(P_{25},P_{75})$ ]	5.3 (4.9, 5.5)	7.0 (6.3, 8.4)	$<$ 0.001	$-$ 5.678 ${}^{*}$
Handgrip strength [kg, $M(P_{25},P_{75})$ ]	19.5 (17.6, 27.4)	20.5 (18.6, 25.8)	0.508	$-$ 0.661 ${}^{*}$
Gait speed (m/s)	0.6 $\pm$ 0.2	0.8 $\pm$ 0.3	0.005	$-$ 2.877 ${}^{\#}$
ODI
Pre-operation	50.4 $\pm$ 8.3	47.3 $\pm$ 6.7	0.081	1.771 ${}^{\#}$
Final	35.0 $\pm$ 6.2	25.1 $\pm$ 6.4	$<$ 0.001	5.487 ${}^{\#}$
Improvement rate (%)	30.5 $\pm$ 11.9	47.3 $\pm$ 10.7	$<$ 0.001	$-$ 5.075 ${}^{\#}$
VAS for back pain [ $M(P_{25},P_{75})$ ]
Pre-operation	5.0 (4.0, 6.0)	6.0 (5.0, 6.0)	0.298	$-$ 1.042 ${}^{*}$
Final	1.5 (1.0, 2.8)	2.0 (1.0, 3.0)	0.400	$-$ 0.842 ${}^{*}$
Improvement rate (%)	71.0 (50.0, 80.0)	67.0 (50.0, 80.0)	0.448	$-$ 0.758 ${}^{*}$

SP: sarcopenia; NSP: non-sarcopenia; SMI: skeletal muscle mass index; ODI: Oswestry Disability Index; VAS: visual analog scale; ${}^{*}$ : Z score; ${}^{\#}$ : t score.

Table 3

Correlation of parameters of sarcopenia and patient-reported outcome scores

	Values
	ODI		VAS
SMI
Male	$R^{2}=$ 0.5333	$P<$ 0.001	$R^{2}=$ 0.0177	$P=$ 0.491
Female	$R^{2}=$ 0.5504	$P<$ 0.001	$R^{2}=$ 0.0382	$P=$ 0.227
Handgrip strength
Male	$R^{2}=$ 0.0396	$P=$ 0.301	$R^{2}=$ 0.0916	$P=$ 0.111
Female	$R^{2}=$ 0.0002	$P=$ 0.927	$R^{2}=$ 0.0173	$P=$ 0.419
Gait speed
Male	$R^{2}=$ 0.2681	$P=$ 0.004	$R^{2}=$ 0.0097	$P=$ 0.611
Female	$R^{2}=$ 0.2093	$P=$ 0.003	$R^{2}=$ 0.0547	$P=$ 0.136

SMI: skeletal muscle mass index.

Figure 2.

The correlation of the final ODI and VAS scores versus the three parameters of sarcopenia.

SMI ( $P<$ 0.001) and gait speed ( $P=$ 0.005) in the SP group were significantly lower than those in the NSP group, while handgrip strength ( $P=$ 0.508) was similar between the two group (Table 2). With regards to preoperative ODI scores, there was no significant difference (50.4 vs 47.3, $P=$ 0.081) between the two groups. However, the postoperative ODI scores (35.0 vs 25.1, $P<$ 0.001) was much higher and the improvement rate (30.5% vs 47.3%, $P<$ 0.001) was much lower in the SP group when compared to NSP group. The median VAS scores for back pain showed no differences preoperatively (5.0 vs 6.0, $P=$ 0.298) and postoperatively (1.5 vs 2.0, $P=$ 0.400). In addition, the improvement of VAS scores for back pain was similar in the two groups (71.0% vs 67.0%, $P=$ 0.448).

The correlations between the final ODI and VAS scores and SMI, handgrip strength, and gait speed are shown in Fig. 2 and Table 3. The result showed that SMI had a moderate correlation with the final ODI score (male: $r=$ 0.5333, $P<$ 0.001; female: $R^{2}=$ 0.5504, $P<$ 0.001); gait speed had a weak correlation with the final ODI score (male: $R^{2}=$ 0.2681, $P=$ 0.004; female: $R^{2}=$ 0.2093, $P=$ 0.003). However, handgrip strength was not significantly correlated with final ODI score. For VAS score, all 3 parameters of sarcopenia had no correlation with the final results.

To identify independent risk factors for the poor clinically improvement at the final follow-up, patients with ODI improvement rate $<$ 40% were categorized into poor clinically improvement group. The result of multiple logistic regression analysis showed that low SMI and low gait speed were independently associated with poor clinical outcomes at the final follow-up following stand-alone LLIF (Table 4).

Table 4

Risk factors for poor clinical improvement identified by logistic regression analysis

Risk factor	OR	95% CI		$P$ value
		Lower	Upper
Low SMI	6.154	1.731	21.873	0.005
Low gait speed	3.388	1.023	11.224	0.046

SMI: skeletal muscle mass index.

4. Discussion

With the aging population, the incidence of degenerative lumbar diseases was apparently increased [24]. Patients with these diseases typically generate high healthcare costs due to the use of imaging, doctor’s visits and surgery. Lumbar fusion is an effective treatment for a variety of degenerative conditions including lumbar stenosis, spondylolisthesis and discogenic back pain [3, 4]. LLIF is a minimally invasive technique developed in order to avoid the complications of traditional anterior or posterior approaches for lumbar interbody fusion [5]. Sarcopenia has been established as an influencing factor for the clinical improvement following lumbar surgery [14]. Our result demonstrated that SMI and gait speed were correlated with the final ODI score; low SMI and low gait speed had a negative clinical impacts on the clinical improvement after stand-alone LLIF. To our knowledge, this is the first study in the literature to specifically evaluate the relationship between sarcopenia and clinical outcomes in patients who underwent stand-alone LLIF.

The prevalence of sarcopenia in patients with spinal disorders have been reported by many studies. Toyoda et al. [14] performed a cross-sectional study to evaluate the incidence of sarcopenia or dynapenia in outpatient clinic for the patients with spinal disorders. The authors described that the respective incidences of the sarcopenia, dynapenia, and normal stages were 16.4%, 26.7%, and 56.9% for males, and 23.7%, 50.9%, and 25.4% for females. In the cross-sectional observational study by Matsuo et al. [25], the prevalence of sarcopenia was found to be 19.7% in a total of 178 patients with lumbar spinal stenosis. In the present study, we demonstrated that the prevalence of sarcopenia was 23.2% in patients with degenerative lumbar diseases, which corroborated the data from the previous studies.

The population presenting of degenerative lumbar diseases is aging, which presents challenges in perioperative risk stratification for the surgeons. Sarcopenia is thought to specific influence the clinical outcomes following lumbar surgery, although the results remain controversial. Toyoda et al. retrospectively reviewed the medical records of 130 patients who were $>$ 65 years and underwent minimally invasive lumbar decompression surgery [14]. They found that the Japanese Orthopaedic Association (JOA) score improved after minimally invasive lumbar decompression surgery even when the patients were diagnosed as being at different stages of sarcopenia; while low physical performance (low gait speed) was independently associated with poor clinical outcomes. In another study, McKenzie et al. retrospectively analyzed 97 consecutive patients who underwent a single level lumbar fusion for degenerative spondylolisthesis [26]. The results showed that there was no significant difference with regards to outcomes when comparing sarcopenic to non-sarcopenic patients undergoing lumbar fusion. They concluded that sarcopenia does not impact the clinical success of lumbar fusion for degenerative spondylolisthesis. Similarly, Charest-Morin et al. [27] also reported that sarcopenia did not predict the occurrence of adverse events, length of stay, discharge home and death in a selected population of elderly patients undergoing simple lumbar spine surgery for degenerative lumbar diseases. In the current study, the result indicated that the postoperative ODI scores were much higher and the improvement rate was much lower in patients with sarcopenia, while the VAS scores for back pain were not different from those for non-sarcopenic patients. It was concluded that sarcopenia may affect the physical performance activity (ODI score) rather than back pain (VAS) after stand-alone LLIF. The specific mechanism of this effect is currently unknown and needs to be examined in further studies.

The present study also showed that there were more female patients with lower BMI in the SP group, which was consistent with a previous study of Toyoda et al. [14]. The authors found that women with lower BMI tend to have a risk factor for sarcopenia in the patients older than 65 years and underwent minimally invasive lumbar decompression surgery. In addition, low SMI and low gait speed were shown to be independent risk factors for the poor clinically improvement at the final follow-up. In 140 patients who underwent surgery for lumbar spinal stenosis, Eguchi et al. found that postoperative outcomes in Roland-Morris Disability Questionnaire scores and pelvic tilt were both inferior in cases of decreased SMI [16]. Gait speed, as a prerequisite for the diagnosis of sarcopenia, has been associated with the health and functional outcomes, mortality, and survival in older adults in several previous studies [28, 29]. It is recommended that gait speed is a prognostic indicator and diagnostic tool for assessing the surgical outcome of degenerative lumbar diseases [15, 30, 31]. It is reported that the comfortable gait speed for normal men and women was 1.20 $\pm$ 0.13 m/s and 1.09 $\pm$ 0.09 m/s respectively, which decreased to 0.99 $\pm$ 0.18 m/s and 1.01 $\pm$ 0.24 m/s when accompanied by lumbar spinal stenosis [31]. Bonab et al. revealed that gait speed was significantly decreased in patients with lumbar disc herniation and chronic mechanical low back pain when compared to normal populations [32]. In addition, 74% of the changes in the gait speed were found to be associated with pain intensity. Sakai et al. [15] reported that the incidence of patients with low SMI and low gait speed in 235 patients with lumbar spinal stenosis was 27.2% and 17.9%, respectively. These authors found the gait speed was significantly improved, whereas SMI did not change 1-year postoperatively. Therefore, low SMI and low gait may be two predictive factors for poor clinically improvement following stand-alone LLIF, which can be used as prognostic indicators for poor clinical outcome.

There were some limitations in this study. First, it is a retrospective study, which may have potential collection, observer, and recall bias. Second, the study population is limited in size; particularly the SP group had only 16 patients by the relatively strict definition of sarcopenia. The follow-up periods were also short. Studies with larger populations and longer postoperative follow-up periods are needed to verify the result of this study. Third, there was a significant difference in BMI and female gender in the SP group, which could potentially led to different outcomes. Four, gait speed was taken as a parameter of sarcopenia, while degenerative lumbar diseases itself may lead to low gait speed. Currently, it is difficult to discriminate whether the low gait speed is caused by spinal diseases or sarcopenia.

5. Conclusion

In conclusion, sarcopenia impacts the final clinical outcomes of stand-alone LLIF for lumbar diseases. Low SMI and low gait speed were negative impact factors for the clinical improvement after stand-alone LLIF.

Footnotes

Conflict of interest

The authors have no conflict of interest to report.

Funding

This work was supported by grants from the National Natural Science Foundation of China (81501908), Natural Science Foundation of Zhejiang Province (LY19H060005) and major scientific and technological plan for medicine and health of Zhejiang Province (WKJ-ZJ-1903).

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