https://orcid.org/0000-0003-0924-5883
Abstract 摘要
Purpose 目的
To evaluate if reduced muscle mass, assessed with Computed Tomography (CT), is a predictor of intensive care unit (ICU) hospitalization in COVID-19 patients.
评估通过计算机断层扫描（CT）评估的减少肌肉量是否是 COVID-19 患者重症监护病房（ICU）住院的预测因子。
Methods 方法
In this Institution Review Board approved study, we retrospectively evaluated COVID-19 patients treated in our tertiary center from March to November 2020 who underwent an unenhanced chest CT scan within three weeks from hospitalization.We recorded the mean Hounsfield Unit (Hu) value of the right paravertebral muscle at the level of the 12th thoracic vertebra, the hospitalization unit (ICU and COVID-19 wards), clinical symptoms, Barthel Index, and laboratory findings.Logistic regression analysis was applied to assess if muscle loss (Hu<30) is a predictor of ICU admission and outcome.Fisher’s exact and Student’s tests were applied to evaluate if differences between patients with and without muscle loss occurred (p<0.05).
在这个经过机构审查委员会批准的研究中，我们回顾性评估了 2020 年 3 月至 11 月在我们的三级中心接受治疗的 COVID-19 患者，这些患者在住院后三周内进行了无增强胸部 CT 扫描。我们记录了在第 12 个胸椎水平右侧脊柱旁肌肉的平均哈氏单位（Hu）值，住院单位（ICU 和 COVID-19 病房），临床症状，Barthel 指数和实验室检查结果。应用 Logistic 回归分析评估肌肉丢失（Hu<30）是否是 ICU 入院和结果的预测因子。Fisher 确切性检验和学生 t 检验用于评估是否发生了患有肌肉丢失和未患有肌肉丢失的患者之间的差异（p<0.05）。
Results 结果
One-hundred-fifty patients matched the inclusion criteria (46 females; mean age±SD 61.3±15 years-old), 36 treated in ICU. Patients in ICU showed significantly lower Hu values (29±24 vs 39.4±12, p = 0.001). Muscle loss was a predictor of ICU admission (p = 0.004).Patients with muscle loss were significantly older (73.4±10 vs 56.4±14 years), had lower Barthel Index scores (54.4±33 vs 85.1±26), red blood-cell count (3.9±1 vs 4.6±1×1012L−1), and Hb levels (11.5±2 vs 13.2±2g/l) as well as higher white blood-cell count (9.4±7 vs 7.2±4×109L−1), C-reactive protein (71.5±71 vs 44±48U/L), and lactate dehydrogenase levels (335±163 vs 265.8±116U/L) (p<0.05, each).
150 名符合纳入标准的患者（46 名女性；平均年龄±标准差 61.3±15 岁），36 名在 ICU 接受治疗。ICU 患者显示出显著较低的 Hu 值（29±24 vs 39.4±12，p = 0.001）。肌肉流失是 ICU 入院的预测因子（p = 0.004）。肌肉流失患者明显年龄较大（73.4±10 vs 56.4±14 岁），巴氏指数评分较低（54.4±33 vs 85.1±26），红细胞计数（3.9±1 vs 4.6±1×10 12 L −1 ），Hb 水平（11.5±2 vs 13.2±2g/l）以及白细胞计数较高（9.4±7 vs 7.2±4×10 9 L −1 ），C-反应蛋白（71.5±71 vs 44±48U/L），乳酸脱氢酶水平（335±163 vs 265.8±116U/L）也较高（每个 p<0.05）。
Figures 数字
Citation: Giraudo C, Librizzi G, Fichera G, Motta R, Balestro E, Calabrese F, et al. (2021) Reduced muscle mass as predictor of intensive care unit hospitalization in COVID-19 patients. PLoS ONE 16(6):
e0253433.
https://doi.org/10.1371/journal.pone.0253433IF: 3.7 Q2
引用：Giraudo C，Librizzi G，Fichera G，Motta R，Balestro E，Calabrese F 等（2021 年）减少肌肉质量作为 COVID-19 患者重症监护病房住院的预测因子。PLoS ONE 16（6）：e0253433。https://doi.org/10.1371/journal.pone.0253433IF：3.7 Q2
Editor: Pasquale Abete, Universita degli Studi di Napoli Federico II, ITALY
编辑：Pasquale Abete，那不勒斯费德里科二世大学，意大利
Received: March 24, 2021; Accepted: June 7, 2021; Published: June 17, 2021
收到日期：2021 年 3 月 24 日；接受日期：2021 年 6 月 7 日；发布日期：2021 年 6 月 17 日
Copyright: © 2021 Giraudo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
版权：© 2021 Giraudo 等人。本文是根据知识共享署名许可协议分发的开放获取文章，允许在任何媒介中无限制使用、分发和复制，前提是给予原作者和来源适当的署名。
Data Availability: All relevant data are within the paper and its Supporting Information files.
数据可用性：所有相关数据均包含在论文及其支持信息文件中。
Funding: The authors received no specific funding for this work.
资金：作者在这项工作中没有接受任何特定资金。
Competing interests: The authors have declared that no competing interests exist.
竞争利益：作者声明没有竞争利益存在。
Introduction 介绍
Muscle loss can be investigated by various radiological techniques including dual energy absorptiometry, magnetic resonance imaging (MRI), and computed tomography (CT) [1–6]. The latter which is overall the gold standard for the evaluation of body composition allowing a distinction of different tissues according to the attenuation of the X-ray beam, has been widely used for investigating and quantifying muscle loss not only in the elderly but also in patients who underwent prolonged hospitalization [7–11]. Moreover, in the last years, attention has been devoted to the socioeconomic impact of sarcopenia, as part of the so-called frailty syndrome, to the prognostic role of muscle loss in neoplastic patients as well as to its predictive function for postoperative infections [12, 13]. Regarding infectious diseases, recently, the impact of sarcopenia has started to be addressed also for COVID-19. In fact, researchers called for awareness raising about the occurrence of acute and chronic muscle loss in this group of patients and started to demand for tailored dietary and rehabilitation programs [14, 15].
肌肉流失可以通过各种放射学技术进行调查，包括双能量吸收法、磁共振成像（MRI）和计算机断层扫描（CT）[1-6]。后者是评估身体组成的金标准，可以根据 X 射线束的衰减区分不同组织，不仅在老年人中广泛用于调查和量化肌肉流失，而且在接受长期住院治疗的患者中也被广泛使用[7-11]。此外，近年来，人们开始关注肌无力对社会经济的影响，作为所谓的虚弱综合症的一部分，以及肌肉流失在肿瘤患者中的预后作用，以及其对术后感染的预测功能[12,13]。关于传染病，最近，人们开始讨论肌无力对 COVID-19 的影响。事实上，研究人员呼吁提高对这类患者急性和慢性肌肉流失发生的意识，并开始要求定制的饮食和康复计划[14,15]。
Despite the utility of radiology for evaluating sarcopenia and the fact that worldwide the scientific community is looking for predictors of COVID-19 severity, to-date, imaging-based studies investigating the role of muscle composition in COVID-19 patients were still missing.
尽管放射学在评估肌少症方面很有用，并且全球科学界正在寻找 COVID-19 严重程度的预测因子，但迄今为止，研究 COVID-19 患者肌肉组织在其中扮演的角色的基于影像的研究仍然缺失。
Thus, aim of our study was to evaluate if reduced muscle mass as defined at CT (i.e., <30 Hu) is a predictor of intensive care unit (ICU) hospitalization in COVID-19 patients [3, 4, 16].
因此，我们研究的目的是评估在 CT 中定义的减少肌肉量（即<30 Hu）是否是 COVID-19 患者重症监护病房（ICU）住院的预测因素[3, 4, 16]。
Material and methods 材料和方法
Study design and muscle assessment
研究设计和肌肉评估
An electronic search of the database of our tertiary center was performed to identify patients with COVID-19 (i.e., positive at reverse transcription polymerase chain reaction) treated in our hospital from March 2020 to November 2020. The following inclusion criteria were then applied: i) adult COVID-19 patients (>18 years old) who underwent an unenhanced chest CT scan during the first three weeks of hospitalization; ii) chest CT scan including the paravertebral muscles at the level of the 12th thoracic vertebra; iii) COVID-19 patients treated in intensive care unit (ICU) or COVID-19 wards.
我们的三级中心数据库进行了电子搜索，以识别 2020 年 3 月至 2020 年 11 月在我们医院接受治疗的 COVID-19 患者（即通过逆转录聚合酶链反应检测呈阳性）。然后应用以下纳入标准：i）在住院的头三周内进行了无增强胸部 CT 扫描的成年 COVID-19 患者（>18 岁）；ii）胸部 CT 扫描包括第 12 个胸椎水平的脊柱旁肌肉；iii）在重症监护病房（ICU）或 COVID-19 病房接受治疗的 COVID-19 患者。
The following exclusion criteria were established: i) patients who underwent a CT scan only after three weeks of hospitalization; ii) patients examined only with a contrast enhanced CT scan; iii) pediatric patients (<18 years old).
以下排除标准已建立：i）在住院三周后才接受 CT 扫描的患者；ii）仅接受增强 CT 扫描检查的患者；iii）儿科患者（<18 岁）。
Given the inclusion/exclusion criteria, which do not apply any restrictions in terms of gender, ethnicity, and comorbidities, our sample can be considered representative of a larger population.
根据不涉及性别、种族和合并症的纳入/排除标准，我们的样本可以被认为代表了更大的人群。
Patients or their guardians (i.e., for instance for sedated patients on mechanical ventilators) gave written informed consent to the CT scan as usually performed in clinical practice. Institution Review Board approval (i.e., Ethical Committee of Padova, n. 104n/AO/21) was obtained and written informed consent for participation to the study was waived due to the retrospective nature of the study.
患者或其监护人（例如，对于机械通气的镇静患者）以书面形式同意进行 CT 扫描，通常在临床实践中进行。由于研究的回顾性特质，获得了机构审查委员会批准（即 Padova 的伦理委员会，编号 104n/AO/21），对于参与研究的书面知情同意被豁免。
One radiologist with ten years of experience in musculoskeletal imaging collected the mean Hounsfield Unit (Hu) value of the right paravertebral muscle at the level of the 12th thoracic vertebra using a standardized, circular region of interest (ROI) of 2 cm (Fig 1). All measurements were performed with an open source software (Horos v.3, www.horosproject.org).
一名具有十年肌肉骨骼成像经验的放射科医师使用标准化的圆形感兴趣区域（ROI）在第 12 个胸椎水平收集了右侧脊柱旁肌肉的平均 Hounsfield 单位（Hu）值（图 1）。所有测量均使用开源软件（Horos v.3, www.horosproject.org）进行。
图 1. 一名 59 岁男性 COVID-19 患者的轴向计算机断层扫描图像，入住 COVID-19 病房，展示了肌肉密度测量方法的应用。
A circular 2 cm size region of interest was placed on the right paravertebral muscle at the level of the 12th dorsal vertebra and the mean Hounsfield unit value collected.
在第 12 个胸椎的右侧脊柱肌上放置了一个直径为 2 厘米的感兴趣区域，并收集了平均的哈氏单位值。
Information regarding the unit of hospitalization considering ICU and COVID-19 wards, separately, was recorded. Moreover, we collected demographics (i.e., age and gender), Barthel Index (i.e., ordinal scale to measure the performance in activities of daily living; range 0–100) [17], and clinical symptoms at admission (i.e., fever >37.5° Celsius, any respiratory and gastrointestinal symptoms separately and any other symptom, such as neurological and cutaneous, grouped together) and laboratory findings on the same day of the CT (red (RBC) and white blood cell count (WBC), hemoglobin (Hb), C-reactive protein (CRP), creatine phosphokinase (CPK), aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALP), and lactate dehydrogenase (LDH)).
记录了考虑 ICU 和 COVID-19 病房的住院单位的信息。此外，我们收集了人口统计学数据（即年龄和性别）、Barthel 指数（即用于衡量日常生活活动表现的顺序刻度；范围 0-100）[17]，以及入院时的临床症状（即发热>37.5°C，任何呼吸道和胃肠道症状分开，以及任何其他症状，如神经和皮肤症状，分组在一起）和同一天 CT 检查的实验室检查结果（红细胞计数（RBC）和白细胞计数（WBC），血红蛋白（Hb），C-反应蛋白（CRP），肌酸磷酸激酶（CPK），天冬氨酸氨基转移酶（AST），丙氨酸氨基转移酶（ALT），碱性磷酸酶（ALP）和乳酸脱氢酶（LDH）。
Statistical analyses 统计分析
Descriptive statistics were applied for demographics. We used the binary logistic regression analysis for categorical independent variables to assess if reduced muscle mass, defined as Hu values <30, is a predictor of ICU admission and/or adverse outcome [3, 4, 16]. To further assess the accuracy of muscle Hu values in predicting the type of hospitalization (i.e., ICU or COVID-19 wards) we applied the receiver operating characteristic curve (ROC) and selected as cutoff the Hu value with the highest Youden index.
描述性统计学方法用于人口统计学。我们使用二元逻辑回归分析来评估是否减少肌肉质量（定义为 Hu 值<30）是 ICU 入院和/或不良结果的预测因子[3, 4, 16]。为进一步评估肌肉 Hu 值在预测住院类型（即 ICU 或 COVID-19 病房）方面的准确性，我们应用了受试者工作特征曲线（ROC），并选择具有最高 Youden 指数的 Hu 值作为截断点。
The student’s t-test was applied to assess if any difference regarding age, clinical, and laboratory findings occurred between patients with and without muscle loss while the Fisher’s exact test was used for the categorical variable gender.
学生 t 检验被应用来评估在年龄、临床和实验室结果方面是否存在患有肌肉流失和未患有肌肉流失的患者之间的差异，而费舍尔确切性检验则用于分类变量性别。
To assess the robustness of the measurements, a second reader, with four years of experience in musculoskeletal imaging repeated the extraction of all HU values and the intraclass correlation coefficient (ICC), with average measures, was computed; values >.750 were considered as excellent [18].
为了评估测量结果的稳健性，另一位具有四年肌肉骨骼成像经验的读者重复提取所有 HU 值和计算了平均测量的组内相关系数（ICC）；值>.750 被认为是优秀的[18]。
All statistical analyses were performed using SPSS (IBM SPSS Statistics version 26, IBM Armonk, NY, USA) and applying p<0.05 as level of significance.
所有统计分析均使用 SPSS（IBM SPSS Statistics 版本 26，IBM Armonk，纽约，美国）进行，并将 p<0.05 作为显著性水平。
Results 结果
One-hundred-fifty patients were examined (46 females; mean age±SD 61.3±15 years old). The CT scans were performed on average 5.5±4 days after hospital admission. One-hundred fourteen patients were treated in COVID-19 wards only while 36 were hospitalized in ICU. Among all patients treated in ICU, nine died. Overall 43 patients (28.7%) were affected by reduced muscle mass (i.e., HU < 30), 16 of them hospitalized in ICU. One-hundred- thirty-six patients fully recovered while 14 deceased. Altogether six patients with muscle loss died and four of them were in ICU.
一百五十名患者接受了检查（46 名女性；平均年龄±标准差 61.3±15 岁）。CT 扫描平均在入院后 5.5±4 天进行。一百十四名患者仅在 COVID-19 病房接受治疗，而 36 名患者住院在 ICU。在 ICU 接受治疗的所有患者中，有九人死亡。总体而言，43 名患者（28.7%）受到肌肉质量减少的影响（即 HU < 30），其中 16 人住院在 ICU。一百三十六名患者完全康复，而 14 人死亡。总共有六名肌肉流失的患者死亡，其中四人在 ICU。
Patients in ICU showed significantly lower Hu values (29±24 vs 39.4±12 Hu, p = 0.001) (Fig 2).
ICU 中的患者显示出显著较低的 Hu 值（29±24 vs 39.4±12 Hu，p = 0.001）（图 2）。
图 2. 四名 COVID-19 患者的轴向计算机断层扫描图像。
In particular, in a and b, one 74 years-old female and one 82 years-old male with reduced muscle mass (i.e., < 30 Hounsfield unit) hospitalized in intensive care unit. In c and d, two male patients (54 years old in a and 65 years old in b) hospitalized in COVID-19 wards demonstrating muscle values above the threshold for muscle loss.
特别是，在 a 和 b 中，一名 74 岁的女性和一名 82 岁的男性肌肉减少（即<30 Hounsfield 单位）住院治疗重症监护病房。在 c 和 d 中，两名男性患者（a 中 54 岁，b 中 65 岁）住院治疗 COVID-19 病房，肌肉值高于肌肉流失的阈值。
The logistic regression analysis showed that reduced muscle mass significantly influenced patients’ admission in ICU (p = 0.004). Moreover, the Hu values of muscles showed an overall accuracy of 62.9% in classifying the unit of hospitalization. In particular, a value of 34 Hu showed 71.1% sensitivity and 53% specificity for ICU admission (Fig 3). Muscle loss did not influence the overall outcome (p = 0.224).
逻辑回归分析显示，减少的肌肉质量显著影响患者入住 ICU（p = 0.004）。此外，肌肉的 Hu 值在对住院单位进行分类时显示出总体准确率为 62.9%。特别是，34 Hu 的数值显示出对 ICU 入院的敏感性为 71.1%，特异性为 53%（图 3）。肌肉流失对整体结果没有影响（p = 0.224）。
图 3. 肌肉密度测量在分类住院单位中的准确性。
Receiver operating curve demonstrating the overall performance of muscle densitometry, expressed in Hounsfield unit, in classifying patients requiring hospitalization in intensive care unit (62.9% accuracy).
接收器操作曲线展示了肌肉密度测定的整体性能，以 Hounsfield 单位表示，用于对需要住院治疗的重症监护病人进行分类（62.9%准确率）。
The results of the comparison of demographics, clinical, functional independence, and laboratory findings between patients with and without reduced muscle mass are summarized in Table 1.
将患有和未患有肌肉减少的患者之间的人口统计学、临床、功能独立性和实验室结果进行比较的结果总结在表 1 中。
表 1. COVID-19 患者中有无肌肉流失的人群的人口统计、临床和实验室结果比较。
In particular, patients with muscle loss were significantly older (73.4±10 vs 56.4±14 years old, p<0.001) had lower Barthel Index scores (54.4±33 vs 85.1±26, p<0.001), RBC (3.9±1 vs 4.6±1 10^12/L, p<0.001) and Hb levels (11.5±2 vs 13.2±2 g/L, p<0.001). Moreover, patients with reduced muscle mass showed significantly higher WBC (9.4±7 vs 7.2±4 10^9/L, p = 0.019), CRP (71.5±71 vs 44±48 mg/L, p = 0.009), and LDH values (335±163 vs 265.8±116 U/L, p = 0.008). No further statistically significant difference occurred between patients with and without reduced muscle mass for any other investigated variable (p>0.05, each).
特别是，肌肉流失患者明显年龄较大（73.4±10 vs 56.4±14 岁，p<0.001），巴氏指数得分较低（54.4±33 vs 85.1±26，p<0.001），红细胞（3.9±1 vs 4.6±1 10^ 12 /L，p<0.001）和血红蛋白水平（11.5±2 vs 13.2±2 g/L，p<0.001）。此外，肌肉质量减少患者白细胞（9.4±7 vs 7.2±4 10^ 9 /L，p = 0.019），C-反应蛋白（71.5±71 vs 44±48 mg/L，p = 0.009）和乳酸脱氢酶值（335±163 vs 265.8±116 U/L，p = 0.008）明显较高。对于其他任何调查变量，肌肉质量减少患者与无肌肉质量减少患者之间没有进一步的统计学显著差异发生（p>0.05，每个）。
The Hu measurements showed excellent reliability (ICC = .906, 95%CI .870 –.932).
胡氏测量显示出很好的可靠性（ICC = .906，95%CI .870 –.932）。
Discussion 讨论
This is the first radiological study assessing the role of reduced muscle mass in COVID-19 patients and demonstrating that it has an impact on ICU hospitalization. Although muscle loss did not carry a higher risk of mortality, our results are in line with previous research showing, for instance, that the skeletal muscle index is a predictor of progression in patients with sepsis and sarcopenia a predictor of postoperative infections and prolonged hospitalization in patients with colorectal cancer [13, 19–21]. Moreover, according to our data, the value of 34 Hu, even if slightly above the threshold for the definition of reduced muscle mass, indicates with high sensitivity which patients will be admitted to ICU. This finding suggests that even initial signs of muscle loss may have a significant impact on the severity and course of the disease. The underlying physio-pathological mechanism surely needs to be investigated also taking in account the role of laboratory analyses. In our cohort, the laboratory tests confirmed that patients with reduced muscle mass had a more severe disease (e.g., higher levels of LDH and CRP). Regarding in particular CPK, we found higher values in patients with low muscle mass albeit this difference was not significant. Similarly, an association between high levels of CPK and a worse prognosis and/or more severe disease has been recently described and several cases of COVID-19 induced rhabdomyolysis have been reported [22, 23]. Thus, not only should the potential onset of viral myositis due to the virus or the effect of immune mediated mechanisms be further investigated but also the role of angiotensin-converting enzyme receptors on muscles, which may contribute to the onset of myalgia and muscle loss [15, 22]. Certainly, it has to be underlined that in our cohort patients with reduced muscle mass were significantly older, confirming once more that the elderly are at high risk for a more severe course of the disease.
这是第一项放射学研究，评估了 COVID-19 患者减少肌肉量在 ICU 住院中的作用，并证明它对 ICU 住院有影响。尽管肌肉流失并未增加死亡风险，但我们的结果与先前的研究一致，例如，骨骼肌指数是脓毒症患者病情进展的预测因子，肌肉萎缩是结肠癌患者术后感染和延长住院时间的预测因子。此外，根据我们的数据，即使 34 Hu 的数值略高于减少肌肉量的定义阈值，也能高度敏感地指示哪些患者将被送入 ICU。这一发现表明，即使肌肉流失的初期迹象也可能对疾病的严重程度和病程产生重大影响。底层的生理病理机制当然也需要进行调查，同时考虑实验室分析的作用。在我们的队列中，实验室检测证实，肌肉量减少的患者病情更为严重（例如，LDH 和 CRP 水平更高）。 特别是关于 CPK，我们发现低肌肉量患者的数值较高，尽管这种差异并不显著。同样，最近描述了 CPK 水平较高与更糟的预后和/或更严重疾病之间的关联，并报道了几例 COVID-19 引起的横纹肌溶解症[22, 23]。因此，不仅应进一步调查病毒引起的肌炎或免疫介导机制的潜在发作，还应研究肌肉上的血管紧张素转换酶受体的作用，这可能有助于肌痛和肌肉流失的发作[15, 22]。当然，必须强调的是，在我们的队列中，肌肉量减少的患者明显更年长，再次证实老年人更容易出现更严重疾病过程的高风险。
According to our evidence, during ICU hospitalization, despite all the challenges associated with this type of care, standardized physiotherapy programs based, for instance, on passive motion, rotational therapy, and stretching should be implemented and/or further promoted aiming to reduce the negative effect of prolonged immobilization especially in patients which may already be affected by muscle alteration at admission [24, 25]. Furthermore, longitudinal CT studies and/or research projects taking advantage of bedside techniques like ultrasound, which may guarantee a longitudinal monitoring of muscle loss avoiding all risks of contamination associated with patients’ mobilization/transfer to the radiology unit and reducing the radiation exposure, are expected to provide new insights into our findings [26–29].
根据我们的证据，在重症监护病房住院期间，尽管存在与这种护理类型相关的所有挑战，但应实施和/或进一步推广基于被动运动、旋转疗法和拉伸等标准物理治疗方案，旨在减少长时间固定不动对患者的负面影响，特别是对那些可能已经受到肌肉改变影响的患者[24, 25]。此外，利用床边技术如超声等进行纵向 CT 研究和/或研究项目，可以保证对肌肉流失的纵向监测，避免与患者移动/转移到放射科部门相关的所有污染风险，并减少辐射暴露，预计将为我们的研究结果提供新的见解[26-29]。
Considering the overall social impact of the pandemic, Kirwan et al recently addressed the relationship between reduced muscle mass and COVID-19 on a broader level [30]. In fact, they highlighted that not only hospitalized patients may be affected by muscle loss but also the reduced physical activity due to quarantine, isolation and social distancing may cause a progressive loss of muscle tissue on healthy individuals and underlined the importance of home-based exercise programs [30].
考虑到大流行的整体社会影响，Kirwan 等人最近在更广泛的层面上讨论了减少肌肉量与 COVID-19 之间的关系。事实上，他们强调不仅住院患者可能受到肌肉流失的影响，而且由于隔离和社交距离导致的减少体力活动可能会导致健康个体逐渐失去肌肉组织，并强调了家庭锻炼计划的重要性。
This study is affected by several limits. First, information regarding the impact of prolonged hospitalization on muscles was not collected because it exceeded the aim of the study and during the first phase of the pandemic follow-up CTs were not performed. Further research should certainly be done in this direction to better tailor rehabilitation programs after hospital discharge and avoid/reduce the worse consequences of the frailty syndrome.
本研究受到几个限制的影响。首先，由于超出了研究的目的，并且在大流行的第一阶段没有进行长期住院对肌肉的影响的信息收集，因此没有进行 CT 检查。进一步的研究应当朝着这个方向进行，以更好地定制出院后的康复计划，并避免/减少脆弱综合征的更糟糕后果。
Recent evidence highlighted the role of several biochemical variables, like butyryl-cholinesterase, in the evaluation of sarcopenia but also because of the retrospective study design, we could not include such parameters [31]. Certainly, prospective studies on this topic should aim to a multivariate predicting model.
最近的证据突出了几种生化变量的作用，比如丁酰胆碱酯酶，在肌少症评估中的作用，但也因为回顾性研究设计的原因，我们无法包括这些参数[31]。当然，关于这个主题的前瞻性研究应该致力于建立多变量预测模型。
Muscle composition is usually assessed at the level of the third lumbar vertebra but most of COVID-19 patients undergo chest CT and such an approach would have not been feasible. Nevertheless, several studies already demonstrated that also using paravertebral muscles at the thoracic level provides reliable results [31–34].
肌肉组成通常在第三腰椎的水平上进行评估，但大多数 COVID-19 患者接受胸部 CT 检查，这种方法并不可行。尽管如此，已有几项研究表明，在胸椎水平上也使用脊旁肌肉可以提供可靠的结果。
Last, we did not perform a volumetric evaluation of paravertebral muscles’ composition, but we wanted to propose a method easily feasible in clinical practice. In fact, a circular region of interest can be easily drawn without any particular software of analysis and it is not time consuming. Thus, such an easily collectable information can be inserted in the clinical report also in an emergency setting aiming to provide beneficial information to clinicians and anesthesiologists dealing with COVID-19 patients. Moreover, the proposed approach has been already applied in the literature providing robust results as confirmed by our high reproducibility [3, 4, 9, 35–37].
最后，我们没有对椎旁肌的体积进行评估，但我们希望提出一种在临床实践中容易实现的方法。事实上，可以轻松绘制一个圆形感兴趣区域，而无需任何特殊的分析软件，也不会耗费时间。因此，这样一种易于收集的信息也可以在紧急情况下插入临床报告中，旨在为处理 COVID-19 患者的临床医生和麻醉医生提供有益信息。此外，所提出的方法已经在文献中得到应用，我们的高可重复性也得到了证实。[3, 4, 9, 35–37]。
Conclusions 结论
In conclusion, reduced muscle mass demonstrated to be a predictor of ICU admission in patients affected by COVID-19 and radiologists should not only become aware of this finding but, aiming to improve the quality of the delivered care, should embed this information in their report. We call for larger radiological studies, taking in account also the impact of prolonged hospitalization on the muscle tissue, to establish tailored rehabilitation programs after hospital discharge.
总之，减少肌肉质量被证明是 COVID-19 患者 ICU 入院的预测因素，放射科医师不仅应意识到这一发现，而且为了提高提供护理的质量，应将这些信息融入其报告中。我们呼吁进行更大规模的放射学研究，同时考虑长期住院对肌肉组织的影响，以制定出院后的定制康复计划。
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