Outcomes after extracorporeal life support for COVID-19 myocarditis: an analysis of the Extracorporeal Life Support Organization Registry,Critical Care

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Outcomes after extracorporeal life support for COVID-19 myocarditis: an analysis of the Extracorporeal Life Support Organization Registry
Critical Care ( IF 8.8 ) Pub Date : 2022-08-03 , DOI: 10.1186/s13054-022-04111-z
Joseph E Tonna ₁ , Chuen Seng Tan ₂ , Kasia Hryniewicz ₃ , Ryan P Barbaro ₄ , Daniel Brodie ₅ , Graeme MacLaren ₆

Affiliation

First described early in the pandemic, coronavirus disease 2019 (COVID-19)-associated fulminant myocarditis can present with arrhythmias and cardiogenic shock, but may be treatable with mechanical circulatory support, such as venoarterial (VA) extracorporeal life support (ECLS) [1]. To better characterize severe myocarditis during the COVID-19 pandemic, we analyzed adult patients with severe COVID-19 who received ECLS for cardiac, pulmonary, or combined failure using an international registry.

We calculated the rate of mechanical circulatory support use among patients receiving ECLS for COVID-19, describing patient characteristics and risk factors for mortality. We utilized the Extracorporeal Life Support Organization (ELSO) Registry and extracted data on patients ≥ 18 years old, diagnosed with COVID-19 from January 1, 2020, through March 31, 2021. Data released from ELSO are de-identified, do not meet the definition of Human Subjects Research, and therefore do not require repeat human subjects review.

Among 4792 patients receiving ECLS for COVID-19 (Table 1), 4.9% (234) were supported with VA-ECMO, and 88 patients (1.8%) had acute myocarditis during the study period. Among those with myocarditis, 35% were women (p = 0.092). COVID-19 patients receiving ECLS who were diagnosed with myocarditis (n = 88) were more likely to be managed with cardiac support versus pulmonary support (53% vs. 42%, p < 0.001). Among all patients supported for a cardiac indication, patients with myocarditis had less hypercarbia (PaCO₂: 45 mmHg vs. 66 mmHg; p < 0.001), less hypoxemia (PaO₂: 94 mmHg vs. 80 mmHg; p = 0.078), greater metabolic acidosis (serum bicarbonate 22 mEq/L vs. 28 mEq/L; p < 0.001), lower blood pressure (systolic: 101 mmHg vs. 119 mmHg; p < 0.001), and lower pulse pressure (43 mmHg vs. 55 mmHg; p < 0.001) compared with patients without myocarditis. Death percentages were similar between those with and without myocarditis.

Table 1 Differences in characteristics between COVID-19 patients on ECLS with and without myocarditis

Full size table

We acknowledge limitations to this analysis. The Registry did not require myocardial biopsy to prove myocarditis, and hence, patients may have had myocarditis diagnosed as acutely decreased myocardial function on echocardiography accompanied by elevated cardiac enzymes and/or electrocardiographic changes. To account for potential overdiagnosis of myocarditis, we performed a sensitivity analysis excluding patients coded for acute myocardial infarction (AMI). The results were unchanged.

In summary, among patients with COVID-19 supported with ECLS, a diagnosis of myocarditis was uncommon (1.8%) and mortality was 51%. In context, mortality among ECLS patients in the ELSO Registry for COVID-19 was 37% early in the pandemic, and 52% later [2]. This is compared to 25–42% mortality for critically ill COVID-19 patients without ECLS [3]. Risk factors for death among patients with myocarditis receiving ECLS were increasing age and preexisting diabetes mellitus. These findings are consistent with previously identified mortality risk factors in non-ECLS patients with severe COVID-19 [3].

Our findings are important for a number of reasons. While within many high-income nations, high rates of vaccination have greatly reduced mortality, across the world vaccination rates remain only 60% and the pandemic is not over. Our results are the largest COVID-19 myocarditis case series using ECLS and may inform future outbreaks. Finally, we identified that risk factors for mortality among patients with myocarditis on ECLS are not different than among patients without myocarditis. In conclusion, within the largest international Registry of patients requiring ECLS circulatory support for COVID-19, mortality appears higher than for patients with COVID-19 without ECLS, but no different than those on ECLS with only acute respiratory failure.

Data were analyzed under contract from ELSO and can be requested from ELSO directly.

COVID-19:: Coronavirus disease 2019
ECLS:: Extracorporeal life support
ELSO:: Extracorporeal Life Support Organization
AMI:: Acute myocardial infarction

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The authors would like to thank all ELSO Member Centers who diligently and with much effort collected and submitted high-quality data on patients with COVID-19 during the pandemic.

Dr. Tonna is supported by a Career Development Award from the National Institutes of Health (NIH)/National Heart, Lung, And Blood Institute (K23 HL141596). This study was also supported by the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant UL1TR002538 (formerly 5UL1TR001067-05, 8UL1TR000105 and UL1RR025764). Dr. Barbaro receives support from the NIH unrelated to this work (R01 HL153519). None of the funding sources were involved in the design or conduct of the study, collection, management, analysis or interpretation of the data, or preparation, review, or approval of the manuscript.

Authors and Affiliations

The University of Utah School of Medicine, 30 N 1900 E, 3C127, Salt Lake City, UT, 84132, USA
Joseph E. Tonna
National University of Singapore, Singapore, Singapore
Chuen Seng Tan
Minneapolis Heart Institute, Abbott Northwestern Hospital, Minneapolis, MN, 84132, USA
Kasia Hryniewicz
University of Michigan, Ann Arbor, MI, 84132, USA
Ryan P. Barbaro
Columbia University, New York, NY, USA
Daniel Brodie
Cardiothoracic ICU, National University Hospital, Singapore, Singapore
Graeme MacLaren

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Ryan P. BarbaroView author publications
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Daniel BrodieView author publications
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Contributions

JT, RB, GM, and DB designed the study; JT, CST, KH, RB, GM, and DB conducted the study; JT and CST contributed to data acquisition and analysis; JT was involved in drafting of the manuscript; and all authors revised the article for important intellectual content and had approved the final manuscript for publication. JT had full access to the study data and takes responsibility for the data integrity, accuracy, and integrity of the submission as a whole. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Joseph E. Tonna.

Ethics approval and consent to participate

This was an analysis of fully de-identified data, which is not human subjects research and therefore did not require Institutional Review Board approval.

Consent for publication

Not applicable.

Competing interests

Dr. Tonna is the Chair-elect of the Registry Committee of the Extracorporeal Life Support Organization (ELSO). Dr. Barbaro is the ELSO Registry Chair. Dr. MacLaren serves on the board of directors for ELSO. Dr. Brodie receives research support from ALung Technologies. He has been on the medical advisory boards for Abiomed, Xenios, Medtronic, Inspira, and Cellenkos. He is the President-elect of ELSO and the Chair of the Executive Committee of the International ECMO Network (ECMONet).

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Tonna, J.E., Tan, C.S., Hryniewicz, K. et al. Outcomes after extracorporeal life support for COVID-19 myocarditis: an analysis of the Extracorporeal Life Support Organization Registry. Crit Care 26, 235 (2022). https://doi.org/10.1186/s13054-022-04111-z

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Received: 15 July 2022
Accepted: 21 July 2022
Published: 03 August 2022
DOI: https://doi.org/10.1186/s13054-022-04111-z

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Keywords

Cardiac failure
Respiratory failure
Acute respiratory distress syndrome
Myocardial inflammation

中文翻译：

COVID-19心肌炎体外生命支持后的结果：体外生命支持组织登记处的分析

2019 冠状病毒病 (COVID-19) 相关暴发性心肌炎首次在大流行早期被描述，可表现为心律失常和心源性休克，但可以通过机械循环支持治疗，例如静脉动脉 (VA) 体外生命支持 (ECLS) [1 ]。为了更好地表征 COVID-19 大流行期间的严重心肌炎，我们使用国际登记处分析了因心脏、肺或联合衰竭而接受 ECLS 的重症 COVID-19 成年患者。

我们计算了接受 ECLS 治疗 COVID-19 的患者中机械循环支持的使用率，描述了患者特征和死亡风险因素。我们利用了体外生命支持组织 (ELSO) 登记处，并提取了 2020 年 1 月 1 日至 2021 年 3 月 31 日期间 18 岁以上、被诊断为 COVID-19 的患者的数据。从 ELSO 发布的数据被去识别化，不符合人类受试者研究的定义，因此不需要重复人类受试者审查。

在接受 ECLS 治疗 COVID-19 的 4792 名患者中（表 1），4.9%（234 名）接受 VA-ECMO 支持，88 名患者（1.8%）在研究期间患有急性心肌炎。在心肌炎患者中，35% 为女性（p = 0.092）。接受 ECLS 且被诊断患有心肌炎的 COVID-19 患者（n = 88）更有可能接受心脏支持而不是肺支持（53% 对 42%，p < 0.001）。在所有支持心脏适应症的患者中，心肌炎患者的高碳酸血症较少（PaCO ₂：45 mmHg vs. 66 mmHg；p < 0.001），低氧血症较少（PaO ₂：94 mmHg vs. 80 mmHg；p = 0.078）、代谢性酸中毒加重（血清碳酸氢盐 22 mEq/L 对 28 mEq/L；p < 0.001）、血压降低（收缩压：101 mmHg 对 119 mmHg；p < 0.001）和脉压降低（43 mmHg 与 55 mmHg；p < 0.001）与无心肌炎的患者相比。有和没有心肌炎的患者的死亡率相似。

表 1 患有和不患有心肌炎的 ECLS 患者 COVID-19 患者的特征差异

全尺寸表

我们承认这一分析的局限性。登记处不需要心肌活检来证明心肌炎，因此，患者可能患有心肌炎，因为超声心动图显示心肌功能急剧下降并伴有心肌酶升高和/或心电图变化。为了解释心肌炎的潜在过度诊断，我们进行了敏感性分析，排除了编码为急性心肌梗死 (AMI) 的患者。结果没有改变。

总之，在 ECLS 支持的 COVID-19 患者中，心肌炎的诊断并不常见（1.8%），死亡率为 51%。在此背景下，ELSO 登记处 COVID-19 的 ECLS 患者的死亡率在大流行初期为 37%，之后为 52% [2]。相比之下，没有 ECLS 的危重 COVID-19 患者的死亡率为 25-42% [3]。接受 ECLS 的心肌炎患者死亡的危险因素是年龄增加和既往糖尿病。这些发现与先前确定的非 ECLS 重症 COVID-19 患者的死亡风险因素一致 [3]。

我们的发现很重要，原因有很多。虽然在许多高收入国家，高疫苗接种率大大降低了死亡率，但全世界的疫苗接种率仍然只有 60%，而且大流行还没有结束。我们的结果是使用 ECLS 的最大 COVID-19 心肌炎病例系列，可能会为未来的爆发提供信息。最后，我们发现 ECLS 心肌炎患者死亡的危险因素与没有心肌炎的患者没有差异。总之，在需要 ECLS 循环支持 COVID-19 的最大国际患者登记处，死亡率似乎高于没有 ECLS 的 COVID-19 患者，但与仅急性呼吸衰竭的 ECLS 患者没有区别。

数据是根据 ELSO 的合同进行分析的，可以直接向 ELSO 索取。

新冠肺炎：: 2019冠状病毒病
ECLS：: 体外生命支持
其他：: 体外生命支持组织
AMI：: 急性心肌梗塞

Salamanca J、Díez-Villanueva P、Martínez P、Cecconi A、González B、de Marcos G、Reyes CS、Segovia J、Jiménez-Borreguero LJ、Alfonso F. COVID-19“暴发性心肌炎”通过临时机械循环支持成功治疗。JACC 心血管成像。2020；13（11）：2457-9。https://doi.org/10.1016/j.jcmg.2020.05.003。
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Barbaro RP、MacLaren G、Boonstra PS、Combes A、Agerstrand C、Annich G、Diaz R、Fan E、Hryniewicz K、Lorusso R 等。COVID-19 的体外膜肺氧合：国际体外生命支持组织登记处不断演变的结果。柳叶刀。2021；398（10307）：1230-8。
CAS 文章谷歌学术
网络 C-IGobotR。C-ICUI：4244 名 COVID-19 危重成人的临床特征和第 90 天结果：一项前瞻性队列研究。重症监护医学。2021；47（1）：60-73。
文章谷歌学术

下载参考资料

作者要感谢所有 ELSO 会员中心，他们在大流行期间努力收集并提交了有关 COVID-19 患者的高质量数据。

Tonna 博士获得了美国国立卫生研究院 (NIH)/国家心肺血液研究所 (K23 HL141596) 的职业发展奖的支持。这项研究还通过授予 UL1TR002538（原 5UL1TR001067-05、8UL1TR000105 和 UL1RR025764）获得了美国国立卫生研究院国家研究资源中心和国家转化科学推进中心的支持。Barbaro 博士获得了与这项工作无关的 NIH 的支持 (R01 HL153519)。没有任何资金来源参与研究的设计或实施、数据的收集、管理、分析或解释，或手稿的准备、审查或批准。

作者和附属机构

犹他大学医学院, 30 N 1900 E, 3C127, Salt Lake City, UT, 84132, USA
约瑟夫·E·托纳
新加坡国立大学，新加坡，新加坡
全生谭
明尼阿波利斯心脏研究所，雅培西北医院，明尼阿波利斯，明尼苏达州，84132，美国
卡西亚·赫里涅维奇
密歇根大学，安娜堡，密歇根州，84132，美国
瑞安·P·巴巴罗
哥伦比亚大学，纽约，纽约，美国
丹尼尔布罗迪
新加坡国立大学医院心胸重症监护室
格雷姆麦克拉伦

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贡献

JT、RB、GM 和 DB 设计了这项研究；JT、CST、KH、RB、GM 和 DB 进行了研究；JT 和 CST 为数据采集和分析做出了贡献；JT 参与了手稿的起草；并且所有作者都对文章进行了重要的知识性修改，并批准了最终稿件的出版。JT 可以完全访问研究数据，并对整个提交的数据完整性、准确性和完整性负责。所有作者阅读并认可的终稿。

通讯作者

Joseph E. Tonna 的通信。

伦理批准和同意参与

这是对完全去识别化数据的分析，这不是人类受试者研究，因此不需要机构审查委员会的批准。

同意发表

不适用。

利益争夺

Tonna 博士是体外生命支持组织 (ELSO) 注册委员会的候任主席。Barbaro 博士是 ELSO 登记处主席。MacLaren 博士是 ELSO 的董事会成员。Brodie 博士获得 ALung Technologies 的研究支持。他曾在 Abiomed、Xenios、Medtronic、Inspira 和 Cellenkos 的医疗顾问委员会任职。He is the President-elect of ELSO and the Chair of the Executive Committee of the International ECMO Network (ECMONet).

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