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ADULT – Original Submission| Volume 35, ISSUE 1, P77-85, March 2023

Impact of Sarcopenia on Outcomes of Minimally Invasive Cardiac Surgery

  • Mi Hee Lim
    Affiliations
    Cardiovascular Center, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan-si, Gyeongsangnam-do, Korea
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  • Chee-Hoon Lee
    Affiliations
    Cardiovascular Center, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan-si, Gyeongsangnam-do, Korea
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  • Min Ho Ju
    Affiliations
    Cardiovascular Center, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan-si, Gyeongsangnam-do, Korea
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  • Hyung Gon Je
    Correspondence
    Address reprint requests to Hyung Gon Je, MD, PhD, Department of Cardiovascular and Thoracic Surgery, Pusan National University Yangsan Hospital, 20, Geumo-ro, Mulgeum-eup, Yangsan-si, Gyeongsangnam-do 50612, Korea.
    Affiliations
    Cardiovascular Center, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan-si, Gyeongsangnam-do, Korea
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Open AccessPublished:November 12, 2021DOI:https://doi.org/10.1053/j.semtcvs.2021.11.005
      Sarcopenia is an objective marker of poor outcome following cardiac surgery through median sternotomy. However, the clinical impact of sarcopenia after minimally invasive cardiac surgery (MICS) has not been well established. This study aimed to analyze the influence of sarcopenia on the early and late outcomes following MICS. We retrospectively examined 1248 patients who underwent MICS via right mini-thoracotomy or upper sternotomy between February 2009 and April 2020. Patients older than 65 years who underwent preoperative computed tomography were enrolled. Sarcopenia was defined as the lowest sex-specific quartile of the body surface area adjusted psoas muscle area. The early operative and late survival outcomes were compared, and the predictor of late composite outcome was analyzed using Cox proportional regression model. Early and late composite outcomes in both groups were also compared. A total of 367 patients were classified into the sarcopenia (n = 92) or non-sarcopenia (n = 275) group. Patients in the sarcopenia group were older, and had lower preoperative hemoglobin and albumin levels. They had higher estimated surgical mortality, but similar early mortality and major morbidity. The survival and late composite outcome were comparable between the two groups. Sarcopenia was neither an independent predictor of late death nor a composite outcome in the multivariable model. After MICS, patients with sarcopenia displayed comparable perioperative outcomes and survival. The clinical impact of sarcopenia on postoperative outcomes might be alleviated by MICS and early recovery protocol after MICS. MICS could be a reasonable approach for elderly patients with sarcopenia.

      Graphical Abstract

      Keywords

      Abbreviations:

      AF (atrial fibrillation), BSA (body surface area), CPB (cardiopulmonary bypass), CT (computed tomography scan), ICS (intercostal space), ICU (intensive care unit), MICS (minimally invasive cardiac surgery), NYHA (New York Heart Association), PMA (psoas muscle area)
      Unlabelled image
      The Kaplan–Meier Curves of Survival After MICS in the Sarcopenia and Non-sarcopenia Groups
      Central Message
      The clinical impact of sarcopenia on postoperative outcomes might be alleviated by MICS and early recovery protocol after MICS. MICS could be a reasonable approach for elderly with sarcopenia.
      Perspective Statement
      Sarcopenia did not significantly affect the early and late clinical outcomes, unlike previously reported results for the conventional sternotomy approach. MICS may mitigate the impact of sarcopenia through its sternal preserving effect and can be a reasonable approach for elderly patients with sarcopenia.

      INTRODUCTION

      Recent studies have reported that patients with sarcopenia who undergo heart surgery through the median sternotomy demonstrate lower survival rates and higher complication rates.
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Okamura H
      • Kimura N
      • Tanno K
      • et al.
      The impact of preoperative sarcopenia, defined based on psoas muscle area, on long-term outcomes of heart valve surgery.
      Although sarcopenia is associated with poor prognosis after cardiac surgery with full sternotomy,
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Yuenyongchaiwat K
      • Kulchanarat C
      • Satdhabudha O.
      Sarcopenia in open heart surgery patients: A cohort study.
      the impact of sarcopenia in cases of minimally invasive cardiac surgery (MICS) is not yet well known. This is partly attributable to the lack of appropriate data because MICS had been prudently performed among older adult patients under various precautions. The relatively longer cardiopulmonary bypass (CPB) and cross-clamp times of MICS also hindered the general application of MICS in older adult patients with sarcopenia.
      • Iribarne A
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      • Russo MJ
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      Comparative effectiveness of minimally invasive versus traditional sternotomy mitral valve surgery in elderly patients.
      Sarcopenia is characterized by loss of skeletal muscle mass in older adults
      • Kiriya Y
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      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
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      and can also be related to malnutrition, low levels of physical activity, and various chronic diseases.
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      ,
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      Sarcopenia.
      These vulnerable general conditions increase the incidence of adverse postoperative outcomes.
      • Yuenyongchaiwat K
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      Sarcopenia in open heart surgery patients: A cohort study.
      The intensive care unit (ICU) stay can also be prolonged, further leading to a decrease muscle mass as part of a vicious cycle.
      • Looijaard WG
      • Dekker IM
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      Skeletal muscle quality as assessed by CT-derived skeletal muscle density is associated with 6-month mortality in mechanically ventilated critically ill patients.
      ,
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      Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients.
      MICS has several advantages of preserving the bone of the thorax, unlike conventional cardiac surgery through median sternotomy. MICS may enhance the patients’ postoperative physical activity by sternal preservation.
      • Dieberg G
      • Smart NA
      • King N.
      Minimally invasive cardiac surgery: A systematic review and meta-analysis.
      Interestingly, MICS performed for slender and frail patients, such as Asians with sarcopenia, often allows for improved surgical visualization for the surgeon, as the distance from the thoracotomy site to the heart valve is shorter in such patients.
      With the super-aging society, the number of patients with sarcopenia requiring heart surgery is also increasing.
      • Xue QL.
      The frailty syndrome: Definition and natural history.
      In addition, the prevalence of sarcopenia is higher in Asian regions, including Korea and Japan, than in Western countries.
      • Beaudart C
      • Rizzoli R
      • Bruyère O
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      Sarcopenia: Burden and challenges for public health.
      Although sarcopenia is widely recognized as a risk factor for functional limitation, physical disability, and decreased quality of life,
      • Beaudart C
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      Sarcopenia: Burden and challenges for public health.
      it remains unclear to what extent sarcopenia affects patients undergoing MICS.
      The motivation for this study was to generate clinical awareness of an improved postoperative condition after MICS in slim, geriatric patients. Older, slender, and more frail patients showed good early postoperative outcomes and remained well during long-term follow-up. Based on these experiences, we hypothesized that sarcopenia had less influence on the patient's postoperative course after MICS, unlike that after full sternotomy.

      MATERIALS AND METHODS

      This retrospective study was based on our institutional database. Between February 2009 and April 2020, a total of 1248 patients underwent MICS via thoracotomy or upper sternotomy. To investigate the clinical impact of sarcopenia in elderly patients, we enrolled 367 patients who were older than 65 years and underwent preoperative computed tomography (CT), which included abdominal CT, to assess sarcopenia (Fig. 1).
      Bilateral psoas muscle areas (PMAs) were measured at the top of the iliac crest on a horizontal plane and averaged. All images were independently reviewed by two researchers to measure the PMA. The areas were automatically calculated by drawing the outline of the psoas muscles using the Infinitt Healthcare (Seoul, Korea) software (Fig. 2). The PMA index was divided by the body surface area to compensate for the influence of the patient's physique on PMA. The patients who had the lowest sex-specific quartile of the PMA index were classified into the sarcopenia group in accordance with previously established methodologies.
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Okamura H
      • Kimura N
      • Tanno K
      • et al.
      The impact of preoperative sarcopenia, defined based on psoas muscle area, on long-term outcomes of heart valve surgery.
      ,
      • Amini N
      • Spolverato G
      • Gupta R
      • et al.
      Impact total psoas volume on short- and long-term outcomes in patients undergoing curative resection for pancreatic adenocarcinoma: A new tool to assess sarcopenia.
      • Ganapathi AM
      • Englum BR
      • Hanna JM
      • et al.
      Frailty and risk in proximal aortic surgery.
      • Mok M
      • Allende R
      • Leipsic J
      • et al.
      Prognostic value of fat mass and skeletal muscle mass determined by computed tomography in patients who underwent transcatheter aortic valve implantation.
      • Peng P
      • Hyder O
      • Firoozmand A
      • et al.
      Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma.
      This study was approved by our Institutional Review Board (approved December 22, 2020, approval 05-2020-253). Informed consent was waived owing to the retrospective study design.
      Figure 2
      Figure 2The psoas muscle area (PMA) was automatically calculated by drawing the outline of the psoas muscles. The PMA index in a fragile patient with sarcopenia (A) was 256.6 mm2/m2 and that in a muscular patient without sarcopenia (B) was 961.8 mm2/m2. The distribution of psoas muscle area measured at the level of the top the iliac crest (C).

      Surgical Procedure

      The right anterior mini-thoracotomy approach through the right second or third intercostal space (ICS) and partial sternotomy were used for isolated aortic valve replacement depending on the position of the ascending aorta. The right anterolateral mini-thoracotomy through the fourth ICS was used for the mitral valve and tricuspid valve.
      Cannulation was established via the femoral artery and vein in most patients who underwent MICS via thoracotomy. During femoral artery cannulation, we attempted to confirm that the guidewire entered up to the mid-thoracic level of the descending thoracic aorta through real-time transesophageal echocardiography guidance performed by an anesthesiologist. In cases of grade 3 or 4 atherosclerosis of the aorta detected using preoperative CT, we altered our perfusion strategy from femoral artery to ascending aorta through an upper sternotomy.
      • Barazangi N
      • Wintermark M
      • Lease K
      • et al.
      Comparison of computed tomography angiography and transesophageal echocardiography for evaluating aortic arch disease.
      Additional venous cannulation to the superior vena cava was performed either directly in the surgical field or through the right internal jugular vein, as in a previous MICS study.
      • Lee CH
      • Kwon Y
      • Park SJ
      • et al.
      Comparison of del Nido and histidine-tryptophan-ketoglutarate cardioplegic solutions in minimally invasive cardiac surgery.
      All cardiac procedures were performed under mild hypothermia (29°C-34°C).

      Early Recovery Protocol After MICS

      Anesthesia was induced using propofol, rocuronium, and remifentanil and maintained using sevoflurane and remifentanil. The infusion of rocuronium was routinely stopped when the aortic cross-clamp was released. After discussion between the surgeon and anesthesiologist, on-table extubation was attempted whenever possible. Standard procedures require that the ventilatory status should be assessed, and the standard criteria for extubation should be satisfied. Proper oxygenation should be ensured (saturation >92% or PaO2 > 60 mmHg), and arterial blood gas analysis confirmed that there was no acidosis (pH > 7.25). Sugammadex (Bridion, MERCK Connect), a neuromuscular block reversal agent, was infused immediately after skin closure. After confirming not only complete reversal from neuromuscular blockage but also hemodynamic and clinical stability, extubation was performed. Extubated patients drank water orally after 2 hours and ate after 6 hours. Patients with stable hemodynamics were routinely transferred to the general ward on the next day and began early ambulation.

      Study End Point

      The outcome variables were in-hospital surgery-related morbidities and survival. Analysis of risk factors influencing long-term survival was also conducted. Postoperative morbidities were defined using standard STS data element definitions.

      Surgeons SoT. STS Adult Cardiac Surgery Database. 2019 17 September. Available at: https://www.sts.org/registries-research-center/sts-national-database/sts-adult-cardiac-surgerydatabase. Accessed April, 2021

      Early mortality was defined as death within 30 days of surgery. These patients’ survival and death date were confirmed through the National Health Insurance data. For patients who died, medical records were reviewed if they died at our center, and if not, the cause of death was recorded through a phone call with the bereaved family.
      To analyze the effect of sarcopenia on the early clinical outcome, both early death and early composite outcomes were compared between the two groups. Requirement of prolonged ventilation (>24 h), reoperation for bleeding, major neurological injuries, and acute renal failure were included in the analysis as early composite outcomes. We compared the long-term survival and late composite outcome of patients in the two groups, with early and late death, disabling stroke, and re-hospitalization as a late composite outcome.

      Statistical Analysis

      Categorical variables are presented as frequencies and percentages, and continuous variables are expressed as mean ± SD or median with ranges. Between-group comparison for categorical variables was performed with the chi-square and Fisher's exact test. Student's t-test or the Mann-Whitney U test was used for comparison of the continuous variables.
      Late survival was evaluated using the Kaplan-Meier method. To determine whether sarcopenia influences early and late survivals, we built univariable and multivariable models based on the entire study cohort. Factors found to trend toward significance in univariable testing (P < 0.10) were entered into a multivariable analysis. Binary logistic regression analysis of predictor variables for early mortality and early composite outcome was performed.
      A Cox-multivariable proportional hazards regression model was developed to identify independent predictors of overall mortality and late composite outcome. Entry and removal criteria were P < 0.05 and P > 0.2, respectively. The results of the Cox-regression analysis were plotted using the mean of the covariates. To test for proportional hazard, Schoenfeld residuals were checked (Fig. E1-2).
      All statistical analyses were performed with R version 3.4.2 (R Project for Statistical Computing, Vienna, Austria). All reported P values are two-sided, and P values <0.05 were considered significant.

      RESULTS

      Patients’ Characteristics

      The 367 patients were classified into either the sarcopenia (n = 92) or non-sarcopenia (n = 275) group (Fig. 1). The patients in the lowest sex-specific quartile of the PMA index were classified into the sarcopenia group. Based on the definition of sarcopenia in this study, the cutoff value of PMA index for sarcopenia was 556.2 mm2/m2 for men and 363.6 mm2/m2 for women. The distribution of the PMA index is shown in Figure 2C.
      The median patient age was 72 years (interquartile range [IQR], 68-77), and 220 patients were female (59.9%). Preoperative patient characteristics are shown in Table 1. The patients in the sarcopenia group were older (74.4 ± 5.2 vs 72.1 ± 5.4, years, P < 0.001) and, had higher estimated surgical mortality calculated with EuroSCORE II (4.0% [2.5; 6.5] vs 2.9% [1.6; 6.2], P = 0.042). Additionally, the levels of hemoglobin (11.6 ± 2.0 vs 12.2 ± 1.9, g/dL, P = 0.006) and albumin (3.8 ± 0.5 vs 4.0 ± 0.5, g/dL, P = 0.001) were lower in the sarcopenia group. The PMA index was significantly smaller in the sarcopenia group than in the non-sarcopenia group (382.2 ± 95.8 vs 556.2 ± 123.2,mm2/m2, P < 0.001) (Table 1).
      Table 1Preoperative Patient Characteristics
      Variables: Mean ± SD or Number (Frequency, %) or Median [IQR]Sarcopenia Group (n = 92)Non-sarcopenia Group (n = 275)P-value
      Average PMA (mm2)612.1 ± 194.4895.6 ± 265.1<0.001
      PMA index (mm2/m2)382.2 ± 95.8556.2 ± 123.2<0.001
      Age (y)74.4 ± 5.272.1 ± 5.4<0.001
      Sex (female)55 (59.8)165 (60.0)1.000
      Body surface area (㎡)1.6 ± 0.21.6 ± 0.20.726
      Body mass index (kg/㎡)23.1 [21.0; 24.8]23.5 [21.6; 25.6]0.208
      Weight (kg)57.8 [49.5; 65.0]57.7 [51.0; 65.5]0.480
      Height (m)1.57 [1.52; 1.64]1.57 [1.52; 1.65]0.764
      Hypertension71 (77.2)205 (74.5)0.714
      Diabetes mellitus29 (31.5)77 (28.0)0.608
      Atrial fibrillation24 (26.1)80 (29.1)0.599
      EuroSCORE II (%)4.0 [2.5; 6.5]2.9 [1.6; 6.2]0.042
      NYHA functional class0.824
       I7 (7.6)18 (6.5)
       II34 (40.2)126 (45.8)
       III30 (32.6)83 (30.2)
       IV18 (19.6)48 (17.5)
      Left ventricular ejection fraction (%)61.0 ± 9.461.2 ± 9.30.826
      B type natriuretic peptide269.0 [131.5; 545.0]261.0 [107.0; 606.0]0.610
      Creatinine clearance (ml/min)52.1 ± 22.752.9 ± 20.20.747
      Hemoglobin (g/dL)11.6 ± 2.012.2 ± 1.90.006
      Albumin (g/dL)3.8 ± 0.54.0 ± 0.50.001
      Prior cardiac surgery7 (7.6)12 (4.4)0.345
      EuroSCORE, European System for Cardiac Operative Risk Evaluation; NYHA class, New York Heart Association functional class.
      The right mini-thoracotomy approach was used in 317 (86.3%) patients. The surgical approach and types of cardiac surgery were similar between the two groups. Isolated aortic valve replacement was the most frequently performed procedure (n = 165, 45.0%). The rates of multiple valve surgery were comparable in both groups. The cardiopulmonary bypass time and cardiac ischemic time were numerically shorter in the sarcopenia group than in the non-sarcopenia group without significance (Table 2).
      Table 2Operative Profile
      Variables: Mean ± SD or Number (Frequency, %) or Median [IQR]Sarcopenia Group (n = 92)Non-sarcopenia Group (n = 275)P-value
      Incision0.298
       Mini-thoracotomy76 (82.6)241 (87.6)
       Hemi-sternotomy16 (17.4)34 (12.4)
      Aortic valve41 (44.6)124 (45.1)1.000
      Mitral valve21 (22.8)70 (25.5)0.714
      Tricuspid valve5 (5.4)17 (6.2)0.994
      Combined15 (16.3)40 (14.5)0.810
       Aortic valve and mitral valve030.736
       Mitral valve and tricuspid valve15350.490
       Aortic valve and tricuspid valve020.998
      Surgical ablation18 (19.6)78 (28.4)0.127
      Atrial septal defect closure8 (8.7)22 (8.0)1.000
      Cardiac tumor7 (7.6)8 (2.9)0.096
      Cardiopulmonary bypass time (min)106.4 ± 41.4109.1 ± 47.40.624
      Cardiac ischemic time (min)74.8 ± 31.877.6 ± 33.70.496
      Because there is no established method to compensate for the effect of a patient's physique on PMA, the analysis of PMA divided by body mass index was also performed. There was no significant difference in the results analyzed according to the PMA index (Table E1-E3).

      Early Clinical Outcomes

      Nine early deaths (2.5%) occurred, with no significant differences between the two groups (sarcopenia vs non-sarcopenia; 2.2% vs 2.5%, P = 1.000). The early morbidity rates of the groups were comparable. The length of ICU and hospital stays were also similar in both groups (Table 3). In total, 280 (76.3%) patients were transferred to a general ward the day after surgery (sarcopenia vs non-sarcopenia; 72.8% vs 77.5%, P = 0.446).
      Table 3Early Clinical Outcomes. Early Composite Outcomes Include Requirement of Prolonged Ventilation (>24 h), Reoperation for Bleeding, Major Neurological Injuries, and Acute Renal Failure
      Variables: Mean ± SD or Number (Frequency, %) or Median [IQR]Sarcopenia Group (n = 92)Non-sarcopenia Group (n = 275)P-value
      On-table extubation41 (44.6)147 (53.5)0.174
      Ventilation duration >24 h6 (6.5)12 (4.4)1.000
      Pneumonia3 (3.3)7 (2.5)1.000
      Pulmonary complication8 (8.7)22 (8.0)1.000
      Acute renal failure1 (1.1)4 (1.5)1.000
      New-onset dialysis4 (4.3)6 (2.2)0.462
      Low cardiac output syndrome17 (18.5)62 (22.5)0.500
      VIS_Peak14.0 [6.0; 32.5]15.0 [7.2; 30.0]0.736
      Mechanical support0 (0)3 (1.1)0.736
      Stroke1 (1.1)3 (1.1)1.000
      Atrial fibrillation30 (32.6)91 (33.1)1.000
      PPM insertion0 (0)3 (1.1)0.736
      Re-exploration for bleeding3 (3.3)6 (2.2)0.849
      Need for transfusion54 (58.7)132 (48.0)0.098
      Chest tube drain during 12 h (ml)240.0 [170.0; 384.0]280.0 [165.0; 421.5]0.352
      Wound complication2 (2.2)1 (0.4)0.317
      Intensive care unit stay (h)26.0 [23.5; 41.5]25.0 [24.0; 29.0]0.620
      Hospital stay (d)6.5 [5.0; 8.0]6.0 [5.0; 8.0]0.280
      Early mortality2 (2.2)7 (2.5)1.000
      Early composite outcome10 (10.9)21 (7.6)0.454
      PPM, permanent pace maker; VIS, vasoactive inotropic score.
      No inter-group differences were found in the occurrence of pulmonary complication including pneumonia. On-table extubation was performed in 51.2% of the patients, and the rates of on-table extubation were similar in both groups (Table 3). The overall incidence of mechanical ventilation for more than 8 hours after surgery was 18.2% (n = 67), and the incidence of prolonged ventilation over 24 hours was also comparable between the groups (sarcopenia vs non-sarcopenia; 6.5% vs 4.4%, P = 0.096). Among older patients (average age 72 years), the endotracheal tube was removed within 8 hours after cardiac surgery in 83.4% (n = 306). The incidence of postoperative acute renal failure and the need for mechanical support due to low cardiac output syndrome were also similarly low in both groups. There was no difference between the groups in peak vasoactive inotropic score, which is the drug requirement in the ICU.
      We found three independent risk factors associated with early composite outcomes (Table E4); preoperative cerebrovascular disease, creatinine clearance, and level of serum hemoglobin were independent risk factors, whereas sarcopenia was not an independent risk factor of early composite outcomes according to logistic regression analysis.

      Impact of Sarcopenia on Late Outcomes

      Clinical follow-up was completed at a median duration of 28.4 months (IQR, 12.9-50.7 months) for all patients, 25.5 months (IQR, 11.1-55.5 months) for the sarcopenia group, and 29.4 months (IQR, 13.6-50.3 months) for the non-sarcopenia group.
      Among the 358 survivors, late death occurred in 37 (10.3%) patients and late composite outcomes occurred in 75 patients (20.9%). The Kaplan–Meier curves of overall survival and freedom from late composite outcome were similar between the two groups (Fig. 3). Freedom from cardiac death was also similar between the two groups (Fig. E3). To assess the impact of sarcopenia on the long-term outcomes, a multivariable Cox proportional hazard model for survival was generated. The predictors of overall mortality were New York Heart Association functional class 3 or 4 (hazard ratio [HR], 2.04; 95% confidence interval [CI], 1.07-3.88, P = 0.030), preoperative creatinine clearance (HR, 0.97; 95% CI, 0.95-0.98, P < 0.001) and preoperative serum albumin level (HR, 0.50; 95% CI, 0.28-0.89, P = 0.017). The predictors of late composite outcomes were hypertension (HR, 2.72; 95% CI, 1.07-6.91, P = 0.035), preoperative atrial fibrillation (HR, 2.21; 95% CI, 1.01-4.84, P = 0.048), and preoperative serum albumin level (HR, 0.42; 95% CI, 0.24-0.74, P = 0.003; Table 4). Sarcopenia was not an independent risk factor for mortality or late composite outcome.
      Figure 3
      Figure 3Kaplan–Meier curves of overall survival (A) and freedom from late composite outcomes (B) together with 95% confidence interval, are presented. Composite outcomes include all cause death, disabling stroke, and re-hospitalization. The curve was truncated at 6 years.
      Table 4Cox Proportional Hazard Analysis for Independent Risk Factors for Mortality (n = 46) and Late Composite Outcome (n = 84). Composite Outcomes Include all Cause Death, Disabling Stroke, and Re-hospitalization
      VariableUnivariableMultivariable
      HR (95% CI)P-valueHR (95% CI)P-value
      Mortality
      Age, y1.07 (1.02-1.13)0.0051.02 (0.97-1.08)0.426
      Sex (female)0.92 (0.51-1.66)0.790
      Body surface area, ㎡0.42 (0.08-2.12)0.292
      Sarcopenia1.16 (0.61-2.20)0.654
      NYHA class 3 or 42.62 (1.39-4.93)0.0032.04 (1.07-3.88)0.030
      Hypertension3.25 (1.28-8.24)0.0132.52 (0.99-6.45)0.054
      Diabetes1.21 (0.64-2.26)0.562
      Arterial fibrillation3.99 (0.90-17.65)0.068
      Cerebrovascular disease1.82 (0.87-3.80)0.110
      Creatinine clearance, ml/min0.96 (0.95-0.98)<0.0010.97 (0.95-0.98)<0.001
      Hemoglobin, g/dL0.83 (0.72-0.97)0.0201.11 (0.94-1.31)0.231
      Albumin, g/dL0.34 (0.20-0.58)<0.0010.50 (0.28-0.89)0.017
      Previous cardiac surgery1.43 (0.44-4.63)0.549
      Emergency1.78 (0.98-3.22)0.057
      Late composite outcome
      Age, y1.04 (1.00-1.08)0.0391.01 (0.96-1.07)0.679
      Sex (female)0.99 (0.64-1.53)0.973
      Body surface area, ㎡0.55 (0.24-1.25)0.152
      Sarcopenia1.07 (0.66-1.73)0.797
      NYHA class 3 or 41.68 (1.08-2.61)0.0211.16 (0.63-2.12)0.636
      Hypertension2.66 (1.41-5.02)0.0032.72 (1.07-6.91)0.035
      Diabetes1.53 (0.97-2.40)0.066
      Atrial fibrillation2.22 (1.02-4.87)0.0462.21 (1.01-4.84)0.048
      Cerebrovascular disease1.43 (0.84-2.42)0.186
      Creatinine clearance, ml/min0.98 (0.97-0.99)<0.0010.99 (0.98-1.01)0.515
      Hemoglobin, g/dL0.89 (0.82-0.97)0.0080.98 (0.84-1.14)0.757
      Albumin, g/dL0.69 (0.52-0.90)0.0060.42 (0.24-0.74)0.003
      Previous cardiac surgery1.25 (0.51-3.09)0.627
      Emergency1.27 (0.81-2.02)0.295
      NYHA, New York Health Association.

      DISCUSSION

      This study compared the outcomes of MICS between 367 consecutive patients divided into sarcopenia and non-sarcopenia groups. The groups differed in terms of baseline demographics, with higher age, and lower preoperative serum Hb and albumin levels observed in the sarcopenia group. Another important difference was the higher EuroSCORE II in the sarcopenia group than in the non-sarcopenia group. Although considerable differences initially existed between groups, early mortality and morbidity were similar. Multivariable analysis revealed that sarcopenia was not an independent predictor for early or late composite outcomes and death from any cause in patients who underwent MICS (VIDEO 1).
      The definition of sarcopenia has not yet been fully established, and there are no definitive methods or numerical cutoff values for the diagnosis of sarcopenia. The European Working Group on Sarcopenia in Older People has established several criteria for identifying sarcopenia, including those related to both muscle mass and strength.
      • Cruz-Jentoft AJ
      • Baeyens JP
      • Bauer JM
      • et al.
      Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People.
      Various methods for measuring muscle strength were also presented in general. However, there are limitations to accurately assessing muscle strength in patients with New York Heart Association class 3 or 4 heart failure who require heart surgery. It is difficult to determine whether the underestimation of muscle strength is due to sarcopenia or heart disease. Muscle mass also varies depending on the sex, race, age, weight, and height of the patient.
      • Gallagher D
      • Visser M
      • De Meersman RE
      • et al.
      Appendicular skeletal muscle mass: Effects of age, gender, and ethnicity.
      In this study, the effects of race and age on PMA were negligible, as all patients were of Asian descent and over 65 years of age. Therefore, we decided to use the lowest sex-specific quartile of the PMA index to define sarcopenia.
      Several previous attempts have been made to define sarcopenia using the PMA, lumbar muscle area, and thoracic muscle area.
      • Akkoc I
      • Toptas M
      • Yalcin M
      • et al.
      Psoas muscle area measured with computed tomography at admission to intensive care unit: Prediction of in-hospital mortality in patients with pulmonary embolism.
      Among these, the PMA determined using CT is the most widely accepted tool for diagnosing sarcopenia,
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Okamura H
      • Kimura N
      • Tanno K
      • et al.
      The impact of preoperative sarcopenia, defined based on psoas muscle area, on long-term outcomes of heart valve surgery.
      ,
      • Amini N
      • Spolverato G
      • Gupta R
      • et al.
      Impact total psoas volume on short- and long-term outcomes in patients undergoing curative resection for pancreatic adenocarcinoma: A new tool to assess sarcopenia.
      • Ganapathi AM
      • Englum BR
      • Hanna JM
      • et al.
      Frailty and risk in proximal aortic surgery.
      • Mok M
      • Allende R
      • Leipsic J
      • et al.
      Prognostic value of fat mass and skeletal muscle mass determined by computed tomography in patients who underwent transcatheter aortic valve implantation.
      • Peng P
      • Hyder O
      • Firoozmand A
      • et al.
      Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma.
      as PMA has been indicated to be the most powerful predictor of hospital stay among other parameters including lumbar muscle area, and thoracic muscle area.
      • Akkoc I
      • Toptas M
      • Yalcin M
      • et al.
      Psoas muscle area measured with computed tomography at admission to intensive care unit: Prediction of in-hospital mortality in patients with pulmonary embolism.
      ,
      • Zuckerman J
      • Ades M
      • Mullie L
      • et al.
      Psoas muscle area and length of stay in older adults undergoing cardiac operations.
      Previous research indicates that preoperative sarcopenia defined using PMA was associated with poorer long-term outcomes after valve surgery through full sternotomy.
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Okamura H
      • Kimura N
      • Tanno K
      • et al.
      The impact of preoperative sarcopenia, defined based on psoas muscle area, on long-term outcomes of heart valve surgery.
      ,
      • Hawkins RB
      • Mehaffey JH
      • Charles EJ
      • et al.
      Psoas muscle size predicts risk-adjusted outcomes after surgical aortic valve replacement.
      Sarcopenia can be used as one of the objective means for defining frailty,
      • Beaudart C
      • Rizzoli R
      • Bruyère O
      • et al.
      Sarcopenia: Burden and challenges for public health.
      and the surgical outcomes of patients with frailty are inevitably poor.
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Yuenyongchaiwat K
      • Kulchanarat C
      • Satdhabudha O.
      Sarcopenia in open heart surgery patients: A cohort study.
      However, in our study, there was no difference in early death, late death from any cause, and major morbidities. Multivariable analysis revealed that sarcopenia was not an independent predictor for early and late composite outcomes in patients who underwent MICS.
      Along with PMA index, serum albumin level is well known as another marker of frailty. Preoperative hypoalbuminemia is known to increase mortality and morbidity after cardiac surgery.
      • Engelman DT
      • Adams DH
      • Byrne JG
      • et al.
      Impact of body mass index and albumin on morbidity and mortality after cardiac surgery.
      • Koertzen M
      • Punjabi P
      • Lockwood G.
      Pre-operative serum albumin concentration as a predictor of mortality and morbidity following cardiac surgery.
      • Yu PJ
      • Cassiere HA
      • Dellis SL
      • et al.
      Impact of preoperative prealbumin on outcomes after cardiac surgery.
      Consistent with this, in the current study, unlike sarcopenia, preoperative serum albumin level was identified as a significant factor affecting long term survival of patients after MICS. Patients in the sarcopenia group with a low PMA index are presumed to have positive effects such as better surgical visualization during MICS, but in the case of hypoalbuminemia, MICS-related advantage was not observed.
      Longer CPB time is widely accepted as an independent risk factor for surgery-related complications including death after cardiac surgery.
      • Salis S
      • Mazzanti VV
      • Merli G
      • et al.
      Cardiopulmonary bypass duration is an independent predictor of morbidity and mortality after cardiac surgery.
      The small surgical incision of MICS generally limits the surgeon's movement and surgical exposure, resulting in longer CPB time.
      • Dieberg G
      • Smart NA
      • King N.
      Minimally invasive cardiac surgery: A systematic review and meta-analysis.
      The thinner muscle layer of the thorax and the shorter distance from the skin to the heart valves in Asian patients with sarcopenia could provide better surgical visualization during MICS and may help reduce CPB and cardiac ischemic time for these fragile patients. In our study, CPB and cardiac ischemic times were numerically shorter in the sarcopenia group, although this was not statistically significant.
      For critically ill patients admitted to the ICU, muscle mass may affect weaning off of the ventilator, rehabilitation, time to discharge, and return to daily life.
      • Looijaard WG
      • Dekker IM
      • Stapel SN
      • et al.
      Skeletal muscle quality as assessed by CT-derived skeletal muscle density is associated with 6-month mortality in mechanically ventilated critically ill patients.
      ,
      • Weijs PJ
      • Looijaard WG
      • Dekker IM
      • et al.
      Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients.
      A faster time to recovery reduces the likelihood further loss of muscle mass. Early extubation after cardiac surgery was associated with a shorter duration of ICU stay.
      • Gregory AJ
      • Grant MC
      • Manning MW
      • et al.
      Enhanced recovery after cardiac surgery (ERAS Cardiac) recommendations: An important first step-but there is much work to be done.
      ,
      • Baxter R
      • Squiers J
      • Conner W
      • et al.
      Enhanced recovery 5after surgery: A narrative review of its application in cardiac surgery.
      In our study, more than 75% of patients were transferred to a general ward the day after surgery and mobilized early. The rapid recovery from the acute treatment phase after cardiac surgery may have a greater effect on patients with sarcopenia. We believe that the current results in geriatric patients with sarcopenia stem from not only the small incision using MICS but also a multidisciplinary team approach to facilitate early recovery.

      LIMITATIONS

      This study has several limitations. First, this was an observational study; thus, it has inherent limitations of a non-randomized trial. Second, we did not perform perioperative muscle strength and power assessments, which might be clinically significant in sarcopenia. Although the method has been used repeatedly and widely accepted in previous studies,
      • Kiriya Y
      • Toshiaki N
      • Shibasaki I
      • et al.
      Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery.
      ,
      • Okamura H
      • Kimura N
      • Tanno K
      • et al.
      The impact of preoperative sarcopenia, defined based on psoas muscle area, on long-term outcomes of heart valve surgery.
      the definition of sarcopenia according to race, sex, and age is still not standardized. Third, it might be difficult to generalize the positive effect of sarcopenia after MICS in all centers. Because our center has a MICS adoption rate of approximately 90% in valvular surgery, it may be difficult to apply the findings of this study in centers that do not routinely practice MICS or have low MICS adoption rates. Finally, the relatively small sample size reduced the statistical power of comparisons between the groups. In addition, in the case of such small study groups, the cause of death of patients is important, but it was not possible to determine the causes of death for all patients. We hope this study facilitates further extensive, prospective studies to ascertain the correlation between sarcopenia and MICS outcomes.

      CONCLUSION

      This study explored the impact of sarcopenia on the outcomes following MICS among older adult patients. Sarcopenia did not significantly affect the early clinical outcomes, unlike previously reported results for the conventional sternotomy approach (Fig. 4). Sarcopenia was not an independent predictor for late death according to the multivariable analysis. MICS may mitigate the impact of sarcopenia through its sternal preserving effect and can be a reasonable approach for elderly patients with sarcopenia.
      Figure 4
      Figure 4Graphical abstract. Early clinical outcomes were comparable between the groups, and there was no difference in long term survival. Kaplan–Meier curves of overall survival with 95% confidence interval are presented. Sarcopenia has less impact on postoperative outcomes after minimally invasive cardiac surgery.

      Acknowledgments

      None declared

      Supplementary Material

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      Linked Article

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