Impact of Different Sarcopenia Stages on the Postoperative New Osteoporotic Vertebral Compression Fracture After Percutaneous Kyphoplasty

Methods

From January 2017 to December 2018, consecutive patients who underwent percutaneous kyphoplasty (PKP) for osteoporotic vertebral compression fracture (OVCF) at the Spine Surgical Department of our hospital were included in this retrospective study. The inclusion criteria were as follows: (1) first-ever acute or subacute single-level vertebral compression fracture planned to treated with PKP; (2) underwent preoperative plain film radiography, computed tomography (CT), and magnetic resonance imaging; (3) agreed to take part in the study and signed the informed consent. The exclusion criteria included: (1) previous spinal surgery; (2) pathological fracture, including fractures related to malignancy, infection, or other medical conditions; (3) burst fracture with retro-pulsed bony fragment into the spinal canal and accompanied by neurologic signs before surgery; (4) had complication after surgery, including leakage of cement into the spinal canal, or postoperative neurologic deficit; (5) patients concomitant with severe physical disease who could not adhere to the follow-up visits (had American Society of Anesthesiologists grade≧ Ⅳ); (6) use of steroids; (7) residual back pain(VAS ≧ 4 at 1 month after surgery); and (8) refracture of cemented vertebra. All the patients were prescribed 1-alpha-OH Vitamin D3 (0.5 mcg /day), an active Vitamin D supplement and encouraged to take the medication during 1 year follow-up. The patients were routinely followed up monthly in the outpatient department for the first 3 months after the operation and subsequently at 3-month intervals with regular radiologic studies and osteoporotic medications, or at any point when there was recurrent back pain. New symptomatic fractures was defined as a recurrent back pain and confirmed by MRI. If the patients was lost to follow-up, they would be excluded from our study.

Data collection

For each patient enrolled in this study, the following data were collected: (1) the patient demographic and clinical features, including age, sex, body mass index(BMI), hemoglobin concentration (hemoglobin concentration < 120 g/L for men and < 110 g/L for women was defined as anemia), serum albumin concentration (serum albumin < 35 g/L was defined as hypoproteinemia), comorbidity, diabetes, American Society of Anesthesiologists (ASA) grade, nutritional risk screening 2002 (NRS 2002) scores, lumber bone mineral density(BMD); (2) vertebral fracture image characters, including the fracture level, cement leakage into the disk, vacuum clefts, fracture severity grade. Fracture level of T5-T10, T11-L2, and L3-L5 were defined as thoracic, thoracolumbar, and lumbar segments, respectively. Bone cement intervertebral leakage were verified by intraoperative and postoperative X-ray. Vacuum clefts were identified with pre-procedural plain radiography, CT and MR imaging. Fracture severity grade was characterized as mild (20%-25% collapse), moderate (26%-40% collapse), or severe (> 40% collapse) according to the semiquantitative classification of Genant et al [8]. Besides, the percentage of vertebral body height collapse less than 20% was defined as “very mild”.

Definition of different sarcopenia stages:

The European Working Group on Sarcopenia (EWGSOP1) has recommended that sarcopenia be stratified as “presarcopenia,” “sarcopenia,” and “severe sarcopenia,” based on the severity of this condition [7]. Thus, we classified different sarcopenia stages according to three factor (muscle strength, muscle mass, physical performance) of the updated algorithm proposed by European Working Group on Sarcopenia (EWGSOP2) [9]. “Presarcopenia” is characterized by low muscle strength without the reduction of muscle mass or physical performance; “sarcopenia” is characterized by low muscle strength, plus low muscle mass, “severe sarcopenia” is characterized by low muscle strength, plus low muscle mass and low physical performance; and patients who did not have any of these deficiencies were classified as “normal”.

Measurement of muscle strength, muscle mass and physical performance.

A whole body scan for body composition examination was measured with dual energy X-ray absorptiometry (DXA), and appendicular skeletal muscle mass (kg) were recorded. For the EWGSOP2’s defnition, low muscle mass (LMM) was defned as having appendicular skeletal muscle mass less than 7 kg/m² in men and 6 kg/m² in women, respectively [10].

As recommended by the Asian Working Group for Sarcopenia (AWGS), handgrip strength and 6-meter usual gait speed were used for the measurement of muscle strength and physical performance, respectively [11]. Grip strength was measured on the dominant hand using an electronic hand dynamometer (EH101; Camry, Guangdong Province, China). Low handgrip strength was defined as ≤ 26 kg for men and ≤ 18 kg for women; low gait speed was defined as ≤ 0.8 m/s [12]. For the measurement of the 6-m usual gait speed, patients were asked to walk over a 6-m course at their usual speed. Patients were encouraged to mobilize early after PKP, mainly by walking out of bed. These two tests were conducted postoperatively both 1 day and 1 month, and the best value of 3 consecutive tests was recorded. We used the data of 1 month after surgery, and patients with residual back pain (VAS ≧ 4 at 1 month after surgery) was excluded to avoid interfering with measurement, although no new vertebral fractures have been confirmed by MRI in these patients.

Statistical analysis.

The results are expressed as mean ± SD. The Kolmogorov–Smirnov test was used to determine the normality of continuous data. Statistical significance was evaluated using Student's t-test or one-way ANOVA for continuous normally distributed data. For continuous, non-normally distributed data, the Mann-Whitney U test and Kruskal-Wallis tests were used. Categorical data were compared using the Chi-squared test or Fisher exact test. P<0.05 was considered statistically significant.

To evaluate the risk factors for subsequent fractures, all variables associated with vertebral refractures with P < 0.1 from the univariate analyses were entered into multivariate forward COX regression analysis. Furthermore, Kaplan-Meier analysis was used to determine the cumulative recurrence-free rates according to different sarcopenia stages. All statistical analyses were performed with SPSS for Windows, version 21.0(SPSS Inc., Chicago, IL, USA).

Results

A total of 511 consecutively admitted patients with acute or subacute single-level vertebral compression fracture were screened, and 329 met the entry criteria (Fig. 1). Patient characteristics are summarized in Table 1, the mean age of all the patients was 71.26 years, and the majority of patients (n = 274, 83.3%) were female.

Table 1

Patient demographics and clinical characteristics.
Variable	Total (n = 329)	Normal (n = 195)	presarcopenic (n = 67)	Sarcopenic (n = 43)	Severe sarcopenic (n = 24)	P value
Gender Male Female	55 274	30 165	8 59	10 33	7 17	0.149
Age (year)	70.96 ± 8.31	69.54 ± 7.83	70.87 ± 8.31	73.33 ± 9.15	78.54 ± 5.37	0.000*
BMI(kg/m2)	23.07 ± 3.53	23.78 ± 3.45	22.81 ± 3.39	21.76 ± 3.34	20.37 ± 2.94	0.000*
Albumin(g/L)	37.16 ± 3.78	37.38 ± 3.57	37.86 ± 3.92	35.81 ± 4.26	35.76 ± 3.40	0.008*
Hemoglobin(g/L)	125.25 ± 13.68	126.07 ± 13.87	124.97 ± 13.61	122.09 ± 13.20	125.04 ± 13.12	0.390
ASA grade I II III	102 175 52	62 109 24	24 32 11	12 19 12	4 15 5	0.131
NRS 2002 score < 3 ≥ 3	247 82	158 37	49 18	30 13	10 14	0.000*
Diabetes Yes No	57 272	32 163	10 57	13 31	4 20	0.188
A-SMI(kg/m2)	6.55 ± 0.57	6.77 ± 0.44	6.57 ± 0.35	5.92 ± 0.57	5.81 ± 0.57	0.000*
Handgrip strength(kg)	21.30 ± 6.18	24.41 ± 5.19	17.57 ± 2.52	16.88 ± 5.14	14.37 ± 6.44	0.000*
Gait speed	0.98 ± 0.16	1.03 ± 0.13	1.03 ± 0.12	0.91 ± 0.10	0.65 ± 0.11	0.000*
BMD(T-score)	-2.94 ± 1.04	-2.79 ± 0.98	-2.93 ± 1.16	-3.37 ± 1.07	-3.40 ± 0.88	0.001*
Treated vertebral level T5-T10 T11-L2 L3-L5	50 248 31	27 152 16	12 48 7	8 31 4	3 17 4	0.791
vertebral refractures Yes No	72 257	31 164	14 53	14 29	13 11	0.000*
BMI, Body mass index; ASA, American Society of Anaesthesiologists; NRS, nutritional risk screening; A-SMI, appendicular skeletal muscle mass index The one-way ANOVA was used to assess normally distributed variables, the Kruskal-Wallis test was used for non-normally distributed variables. The chi-square test or Fisher’s Exact test was used for categorical variables. *statistically significant difference (P < 0.05).

Based on the diagnostic criteria, 67 (20.4%), 43 (13.1%), and 24 (7.3%) of patients were identified as having “presarcopenia”, “sarcopenia”, and “severe sarcopenia”, respectively, whereas 195 (59.3%) of patients were identified as “normal”. As is shown in Table 1, the handgrip strength, appendicular skeletal muscle mass index, gait speed significantly lower with advancing sarcopenia stages. Gender, ASA grade, diabetes, and hemoglobin, treated vertebral level did not differ significantly between different sarcopenia stages. Patients with sarcopenia and severe sarcopenia were older, and had lower BMI, lower preoperative serum albumin compared with normal patients, but patients with presarcopenia did not. Patients with presarcopenia, sarcopenia and severe sarcopenia had lower BMD than normal patients. The rate of NRS 2002 score ≥ 3 and the refracture rate increased with advancing sarcopenia stages (19.0% vs 26.9% vs 30.2% vs 58.3%; 15.9% vs 20.9% vs 32.6% vs 54.2%, respectively, P = 000).

In our study, 72 patients (21.9%) had a fracture recurrence. Results of univariate and multivariate analyses for factors associated with osteoporotic vertebral compression refracture (OVCRFs) are presented in Table 2. In univariate analysis, several factors were associated with OVCRFs, including female (p = 0.012), advanced age (≥ 75 years, p = 0.004), lower BMD (p = 0.000), and stages of sarcopenia (p = 0.000). Significant differences were not observed in other factors, including BMI, NRS 2002 score, diabetes, hypoproteinemia, Anemia, ASA grade, Vacuum clefts, treated vertebral level and intradiscal cement leakage and fracture severity grade. Multivariate logistic analysis showed that sarcopenia (OR 2.536; 95% CI 1.130–5.692, p = 0.024) and severe sarcopenia ( OR 4.579; 95% CI 1.615–12.968, p = 0.004), not presarcopenia (OR 1.072; 95% CI 0.509–2.258, p = 0.854) were independent risk factor for OVCRF. Female (OR 6.325; 95% CI 2.176–18.368, p = 0.001), age (OR 1.863; 95% CI 1.002–3.464, p = 0.049), and lower BMD (OR 1.736; 95% CI 1.294–2.328, p = 0.000) were other independent predictors for OVCRFs.

Table 2

Univariate and Multivariate Analysis of Factors Associated With new osteoporotic vertebral compression fractures.
	Univariate analysis			Multivariate analysis
Factors	OVCRFs group (n = 72)	Non-OVCRFs group (n = 257)	P value	OR (95% CI)	P value
Gender Male Female	5 67	50 207	0.012*	1 6.325(2.176–18.368)	0.001*
Age (year) ≥ 75 < 75	37 35	85 172	0.004*	1 1.863 (1.002–3.464)	0.049*
BMI(kg/m2) < 18.5 kg/m2 18.5–24 kg/m2 > 24 kg/m2	7 41 24	22 131 104	0.547
NRS 2002 score < 3 ≥ 3	48 24	199 58	0.062
Diabetes Yes No	13 59	44 213	0.853
Hypoproteinemia Yes No	19 53	68 189	0.990
Anemia Yes No	8 64	38 219	0.427
ASA grade I II III	24 35 13	78 140 39	0.664
BMD(T-score)	3.39 ± 1.05	2.82 ± 1.01	0.000*	1.736(1.294–2.328)	0.000*
Vacuum clefts Yes No cleft	19 53	52 205	0.262
Treated vertebral level T5-T10 T11-L2 L3-L5	15 50 7	35 198 24	0.306
Intradiscal cement leakage Yes No	18 54	60 197	0.986
Severity grade Very mild Mild Moderate Severe	20 21 20 11	104 72 56 25	0.180
Stages of sarcopenia Normal Presarcopenia Sarcopenia Severe sarcopenia	31 15 13 13	170 54 24 9	0.000*	1 1.072(0.509–2.258) 2.536(1.130–5.692) 4.579(1.615–12.986)	0.009* 0.854 0.024* 0.004*
BMI, Body mass index; ASA, American Society of Anaesthesiologists; NRS, nutritional risk screening; OR, odds ratio; CI, confidence interval The Independent-Samples T test was used to assess normally distributed variables, and the chi-square test or Fisher’s Exact test was used for categorical variables. Variables with P < 0.1 from the univariate analyses were entered into multivariate forward logistic regression analysis. *statistically significant difference (P < 0.05).

The time to recurrence event was analyzed by Kaplane-Meier survival curves based on stages of sarcopenia. Patients with sarcopenia and severe sarcopenia had a higher risk of recurrence event compared to patients with presarcopenia and normal patients, P < 0.001; Fig. 2).

Discussion

We enrolled a large sample size to identify the OVCF patients with different stages of sarcopenia according to EWGSOP sarcopenia classification by assessing muscle strength, muscle mass and physical performance. The cut-off values of handgrip strength and 6-meter usual gait speed were according to AWGS because of the eastern people generally have a smaller physique and a lower BMI than the western people. To avoid the effects of pain and movement restriction, handgrip strength and 6-meter usual gait speed were measured post-operation.

The relationship between sarcopenia and vertebral compression fractures has been preliminarily explored. Iolascon et al. [13] confirmed that the rate of sarcopenia increasing along with the number of vertebral fragility fractures in women. A cross-sectional study examined 216 women with fresh OVCF, the result showed sarcopenia were independent risk factors for acute OVCF [14]. However, both two studies definition of sarcopenia only included skeletal muscle mass as the unique parameter. Thus, the sarcopenic patients identified by these studies could have presarcopenia, sarcopenia, or severe sarcopenia. One study in community-dwelling elderly subjects showed that elderly subjects with sarcopenia had a greater risk of falls compared with normal elderly subjects, but those with presarcopenia did not [15]. Another study in women with a hip fracture showed that sarcopenic women had a lower ability to function in their activities of daily living than presarcopenic women [16]. These results demonstrated the value of sarcopenia classification for a better risk stratification. A total of 72 (21.9%) recurrent OVCF occurred during our 1-year follow-up and the refracture rate was increased in advancing sarcopenia patients (20.9% vs 32.6% vs 54.2%, respectively). Our multivariate analysis also demonstrated that sarcopenia, severe sarcopenia were independent risk factors for OVCRF, whereas presarcopenia was not.

The reasons why OVCF recurrence rate increased in advanced sarcopenia stage remain uncertain, the following reasons can be hypothesized. First, a large proportion of fragility fractures in patients with osteoporosis are reported to be caused by falls [17]. Muscle mass and strength as critical components in maintaining physical function, mobility, and vitality [18]. Low muscle quality would lead to physical disability and frailty, and subsequently increase the risk of falls. Previous studies have reported patients with sarcopenia over 80 - year - old were approximate three times to have a fall than non-sarcopenia patients within two years [19]. Second, advanced sarcopenia stage was associated with a lower BMD in the present study(Table 1,P = 0.007). Two large sample data study confirmed sarcopenia was associated with osteopenia and osteoporosis in Asian area [20, 21]. For patients with low BMD, the quality of the vertebral bodies was poor, resulting in a greater probability of OVCRF. Bone and muscle are not only adjacent to each other in anatomy, but also indispensable in basic metabolism. Recently, it has become clear that bone and muscle share genetic determinants [22]. The close interaction between bone loss and muscle wasting results in the co-occurrence of osteoporosis and sarcopenia, named osteosarcopenia [23]. Furthermore, some researchers have found a synergistic effect between osteoporosis and sarcopenia, lead to the occur of fragility fracture [24].

Low bone mineral density is another risk factor for recurrent fractures in this study. The average T-score was − 3.4 in patients with subsequent fractures and − 2.8 in patients without subsequent fractures group. Young-Joon Rho et al. [25] regard osteoporosis as the most important risk factor for additional fracture. However, Compared with BMD (OR 1.736; 95% CI 1.294–2.328, p = 0.000), sarcopenia (OR 2.536; 95% CI 1.130–5.692, p = 0.024) and severe sarcopenia (OR 4.579; 95% CI 1.615–12.968, p = 0.004) had greater odds ratio in the multivariate model. We therefore concluded that sarcopenia, severe sarcopenia had much stronger prediction power for the occurrence of postoperative OVCRF than BMD.

Advanced sarcopenia stage was associated with lower BMI (P = 0.000), lower serum albumin level (P = 0.008) and higher NRS 2002 scores (P = 0.000) in the present study(Table 1), both of which are common index to evaluate nutritional status. Lin WC et al reported that low BMI was a significant predictor of new VCFs after vertebroplasty, especially if the BMI was less than 22 kg/m [26]. However, none of the traditional nutritional indices, such as BMI, albumin levels and NRS 2002 scores, were associated with OVCRF. We speculated that sarcopenia is a more comprehensive parameter than these traditional nutritional indices, reflecting not only the nutritional status but also the functional status. Moreover, skeletal muscle mass has been reported to be a new index for nutritional assessment [27]. Existing research has focused more on anti-osteoporosis treatment to prevent recurrence of fractures [28, 29], the present study indicated that anti-sarcopenia could be regarded as a potential therapeutic target in the future. We think resistance training program such as knee extension/flexion and leg presses to offset sarcopenia could be carried out at the appropriate time after surgery. Adequate nutritional intake and certain nutritional supplements, such as leucine and omega-3 polyunsaturated fatty acids, could have a synergistic effect with resistance training in maintaining muscle mass [30].

Age and sex were statistically significant difference between the OVCRFs group and non-OVCRFs group in univariate analysis. Other risk factors like treated vertebral level, vacuum clefts, intradiscal cement leakage, and AP ratio showed no difference between the two groups, which were still controversial [25, 31, 32]. Meanwhile, multivariate analysis revealed that female (OR 6.325; 95% CI 2.176–18.368, p = 0.001) and older age (OR 1.863; 95% CI 1.002–3.464, p = 0.049) were related to OVCRFs after PKP in our study. As people getting older, the quantity and mass of trabeculae will decrease simultaneously. The absorption of calcium in the digestive system decreases at the same time, leading to the loss of bone mass in elderly patients, especially postmenopausal women [33, 34]. Lidsay et al. [35] observed that almost 20% of women would experience another fracture within 1 year of an incident vertebral fracture.

The present study was strengthened by its large sample retrospective study design, the strict inclusion and exclusion criteria, and rigorous follow-up strategy. Our department is one of the largest spine centers in China, performing > 400 OVCF operations annually, which enabled the study to be finished within a short time range. However, there are still several limitations. First, this is a single-center study, the conclusions of this study need to be validated in multicenter studies in the future. Second, only symptomatic subsequent fractures were included. The actual subsequent fractures rate would be higher than the observed rate. Third, there were differences in the use of anti-osteoporosis drugs during postoperative follow-up, which may resulted in a biased refracture rate.

References

Buchbinder R, Johnston RV, Rischin KJ, Homik J, Jones CA, Golmohammadi K, Kallmes DF (2018) Percutaneous vertebroplasty for osteoporotic vertebral compression fracture. Cochrane Database Syst Rev 4:CD006349.
McGirt MJ, Parker SL, Wolinsky JP, Witham TF, Bydon A, Gokaslan ZL (2009) VertebropIasty and kyphopIasty for the treatment of veaebraI compression fractures: an evidenced based review of the Iiterature. Spine J 9:501-508.
Sun G, Tang H, Li M, Liu X, Jin P, Li L (2014) Analysis of risk factors of subsequent fractures after vertebroplasty. Eur Spine J 23:1339–1345.
Kang SK, Lee CW, Park NK, Kang TW, Lim JW, Cha KY, Kim JH (2011) Predictive risk factors for refracture after percutaneous vertebroplasty. Ann Rehabil Med 35:844-851.
Chen LK, Lee WJ, Peng LN, Liu LK, Arai H, Akishita M, Asian Working Group for Sarcopenia (2016) Recent advances in sarcopenia research in Asia: 2016 update from the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 17:767.e1-7.
Wu CH, Yang KC, Chang HH, Yen JF, Tsai KS, Huang KC (2013) Sarcopenia is related to increased risk for low bone mineral density. J Clin Densitom 16:98-103.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M; European Working Group on Sarcopenia in Older People (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412-423.
Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8:1137-1148.
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31.
Costanzo L, De Vincentis A, Di Iorio A, Bandinelli S, Ferrucci L, Antonelli Incalzi R, Pedone C. Impact of Low Muscle Mass and Low Muscle Strength According to EWGSOP2 and EWGSOP1 in CommunityDwelling Older People. J Gerontol A Biol Sci Med Sci. 2020 ;75(7):1324-1330.
Boutin RD, Yao L, Canter RJ, Lenchik L (2015) Sarcopenia: Current Concepts and Imaging Implications. AJR Am J Roentgenol 205: W255-266.
Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, Limpawattana P, Lin CS, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H (2014) Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 15:95-101.
Iolascon G, Giamattei MT, Moretti A, Di Pietro G, Gimigliano F, Gimigliano R (2013) Sarcopenia in women with vertebral fragility fractures. Aging Clin Exp Res Suppl 1:S129-131.
Hida T, Shimokata H, Sakai Y, Ito S, Matsui Y, Takemura M, Kasai T, Ishiguro N, Harada A (2016) Sarcopenia and sarcopenic leg as potential risk factors for acute osteoporotic vertebral fracture among older women. Eur Spine J 25:3424-3431.
Di Monaco M, Castiglioni C, De Toma E, Gardin L, Giordano S, Di Monaco R, Tappero R (2015) Presarcopenia and sarcopenia in hip-fracture women: prevalence and association with ability to function in activities of daily living. Aging Clin Exp Res 27:465-472.
Tanimoto Y, Watanabe M, Sun W, Sugiura Y, Hayashida I, Kusabiraki T, Tamaki J (2014) Sarcopenia and falls in community-dwelling elderly subjects in Japan: Defining sarcopenia according to criteria of the European Working Group on Sarcopenia in Older People. Arch Gerontol Geriatr 59:295-299.
Tsuda T (2017) Epidemiology of fragility fractures and fall prevention in the elderly: a systematic review of the literature. Curr Orthop Pract 28:580-585.
Prado CM, Heymsfield SB (2014) Lean tissue imaging: a new era for nutritional assessment and intervention. JPEN J Parenter Enteral Nutr 38:940-953.
Landi F, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G (2012) Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr 31:652-658.
Miyakoshi N, Hongo M, Mizutani Y, Shimada Y (2013) Prevalence of sarcopenia in Japanese women with osteopenia and osteoporosis. J Bone Miner Metab 31:556-561.
Go SW, Cha YH, Lee JA, Park HS (2013) Association between Sarcopenia, Bone Density, and Health-Related Quality of Life in Korean Men. Korean J Fam Med 34:281-288.
Karasik D, Kiel DP (2008) Genetics of the musculoskeletal system: a pleiotropic approach. J Bone Miner Res 23:788-802.
Hirschfeld HP, Kinsella R, Duque G (2017) Osteosarcopenia: where bone, muscle, and fat collide. Osteoporos Int 28:2781-2790.
Walsh MC, Hunter GR, Livingstone MB (2006) Sarcopenia in premenopausal and postmenopausal women with osteopenia, osteoporosis and normal bone mineral density. Osteoporos Int 17:61-67.
Rho YJ, Choe WJ, Chun YI (2012) Risk factors predicting the new symptomatic vertebral compression fractures after percutaneous vertebroplasty or kyphoplasty. Eur Spine J 21:905-911.
Lin WC, Cheng TT, Lee YC, Wang TN, Cheng YF, Lui CC, Yu CY (2008) New vertebral osteoporotic compression fractures after percutaneous vertebroplasty: retrospective analysis of risk factors. J Vasc Interv Radiol 19:225-231.
Prado CM, Heymsfield SB (2014) Lean tissue imaging: a new era for nutritional assessment and intervention. JPEN J Parenter Enteral Nutr 38:940-953.
Zeng LF, Pan BQ, Liang GH, Luo MH, Cao Y, Guo D, Chen HY, Pan JK, Huang HT, Liu Q, Guan ZT, Han YH, Zhao D, Zhao JL, Hou SR, Wu M, Lin JT, Li JH, Liang WX, Ou AH, Wang Q, Yang WY, Liu J (2019) Does Routine Anti-Osteoporosis Medication Lower the Risk of Fractures in Male Subjects? An Updated Systematic Review With Meta-Analysis of Clinical Trials. Front Pharmacol 10:882.
Bawa HS, Weick J, Dirschl DR (2015) Anti-Osteoporotic Therapy After Fragility Fracture Lowers Rate of Subsequent Fracture: Analysis of a Large Population Sample. J Bone Joint Surg Am 97:1555-1562.
Phillips SM (2015) Nutritional supplements in support of resistance exercise to counter age-related sarcopenia. Adv Nutr 6:452-460.
Lin EP, Ekholm S, Hiwatashi A, Westesson PL (2004) Vertebroplasty: cement leakage into the disc increases the risk of new fracture of adjacent vertebral body. AJNR Am J Neuroradiol 25:175-180.
Lin CC, Chen IH, Yu TC, Chen A, Yen PS (2007) New symptomatic compression fracture after percutaneous vertebroplasty at the thoracolumbar junction. AJNR Am J Neuroradiol 28:1042-1045.
Watts NB (2018) Postmenopausal Osteoporosis: A Clinical Review. J Womens Health (Larchmt) 27:1093-1096.
Edwards MH, Dennison EM, Aihie Sayer A, Fielding R, Cooper C (2015) Osteoporosis and sarcopenia in older age. Bone 80:126-130.
Lindsay R, Silverman SL, Cooper C, Hanley DA, Barton I, Broy SB, Licata A, Benhamou L, Geusens P, Flowers K, Stracke H, Seeman E (2001) Risk of new vertebral fracture in the year following a fracture. JAMA 285:320-323.

Impact of Different Sarcopenia Stages on the Postoperative New Osteoporotic Vertebral Compression Fracture After Percutaneous Kyphoplasty

Abstract

Introduction