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• Author's reply
  Arthur Mageau, Karim Sacré and Jean-François Timsit
  Published on: 7 April 2022
• Correspondence on “Survival after COVID-19-associated organ failure among inpatients with systemic lupus erythematosus in France: a nationwide study” by Mageau et al.
  Tsung-Yuan Yang, Lung-Fa Pan and Gwo-Ping Jong
  Published on: 31 March 2022

• Published on: 7 April 2022

  Author's reply

  • Arthur Mageau, M.D. Département de Médecine Interne, Assistance Publique Hôpitaux de Paris, Hôpital Bichat - Claude-Bernard, Paris, France
  • Other Contributors:
    • Karim Sacré, Professor
    • Jean-François Timsit, Professor

  We thank Tsung-Yuan Yang and colleagues for their interest in our findings on survival after COVID-19 associated organ-failure among SLE population. They raised two interesting questions on the method that we used.
  First, they suspect a selection bias because we selected, for the unmatched analysis, patients still alive at D30 to measure the survival in the D30-D90 period while SLE patients had a lower mortality during the D0-D30 period. They stated that selecting patients based on what the next observation allocation is likely to be can lead to biased estimates. We agree with them, and, as we already wrote in the discussion section, “Such observation may be biased because patients with SLE are younger and more frequently female” which could explain the better prognosis during the D0-D30 period. Besides, we used D30 as a landmark not by choice, but because, in the matched analysis, (Figure 2) the Kaplan-Meier curves crossed at D30, and the proportional hazard assumption was therefore not respected. We did not drive conclusions from this unmatched analysis which was here mainly to show the importance of our matching procedure.
  Second, they raised the concern that “the baseline characteristics between the two groups were not defined in this study”. We partly disagree on this comment. As a matter of fact, we presented in Table 1 (unmatched analysis) and in Table 2 (matched analysis) the baseline characteristic of our studied populations. We presented all the data...

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  We thank Tsung-Yuan Yang and colleagues for their interest in our findings on survival after COVID-19 associated organ-failure among SLE population. They raised two interesting questions on the method that we used.
  First, they suspect a selection bias because we selected, for the unmatched analysis, patients still alive at D30 to measure the survival in the D30-D90 period while SLE patients had a lower mortality during the D0-D30 period. They stated that selecting patients based on what the next observation allocation is likely to be can lead to biased estimates. We agree with them, and, as we already wrote in the discussion section, “Such observation may be biased because patients with SLE are younger and more frequently female” which could explain the better prognosis during the D0-D30 period. Besides, we used D30 as a landmark not by choice, but because, in the matched analysis, (Figure 2) the Kaplan-Meier curves crossed at D30, and the proportional hazard assumption was therefore not respected. We did not drive conclusions from this unmatched analysis which was here mainly to show the importance of our matching procedure.
  Second, they raised the concern that “the baseline characteristics between the two groups were not defined in this study”. We partly disagree on this comment. As a matter of fact, we presented in Table 1 (unmatched analysis) and in Table 2 (matched analysis) the baseline characteristic of our studied populations. We presented all the data that we had regarding the simplified acute physiology score 2 (SAPS 2) which is also a classification tool for individual’s risk mortality in hospital (1) and an analogue of APACHE 2 used in France. However, we acknowledge that this score is only collected in intensive care units (ICUs), so it was available only for patients admitted in these units. As presented in table 2, and even though SAPS 2 was not part of the matching variables, this score was distributed similarly between SLE and non-SLE matched populations.
  Overall, we provide evidence that, after considering age, sex, and several comorbidities, SLE patients have a late-onset poor prognosis after COVID-19 AOF.

  References:
  1-Le Gall J, Lemeshow S, Saulnier F. A New Simplified Acute Physiology Score (SAPS II) Based on a European/North American Multicenter Study. JAMA. 1993;270(24):2957–2963.

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  Conflict of Interest:
  None declared.

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• Published on: 31 March 2022

  Correspondence on “Survival after COVID-19-associated organ failure among inpatients with systemic lupus erythematosus in France: a nationwide study” by Mageau et al.

  • Tsung-Yuan Yang, Cardiology Department of Internal Medicine, Chung Shan Medical University Hospital and Chung Shan Medical University
  • Other Contributors:
    • Lung-Fa Pan, Professor
    • Gwo-Ping Jong, Professor

  We read with great interest the article by Mageau et al.,1 who reported that COVID-19-associated organ failure (AOF) is associated with a poor late-onset outcome between days 30 (D30) and 90 (D90) among patients with systemic lupus erythematosus (SLE) in France. Conversely, they noted that an unchanged survival rate of patients with SLE with COVID-19-AOF will require hospitalization compared with patients without SLE COVID-19-AOF at D90. This study is a valuable addition to the literature. However, we share some concerns about this article to the authors.
  First, the selection bias may be suspect in this study. A selection bias occurs when those in charge of the recruitment or enrollment of patients (recruiters) selectively enroll patients into the study based on what the next observation allocation is likely to be.2 At D30, 43 (21.9%) in-hospital deaths were recorded among patients with SLE with COVID-19-AOF compared with 31,274 (27.6%) in the unmatched patients without SLE with COVID-19-AOF. At baseline (D30), they may enroll a sick patient in patients with SLE with COVID-19-AOF compared with patients without SLE with COVID-19-AOF. This strategy can lead to substantially biased estimates of the survival of patients with COVID-19-AOF between D30 and D90 and misleading conclusions.
  Second, prior studies have shown numerous AOFs, and disease severity of COVID-19 is independently associated with the increased risk of mortality.3,4 Furthermore, several para...

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  We read with great interest the article by Mageau et al.,1 who reported that COVID-19-associated organ failure (AOF) is associated with a poor late-onset outcome between days 30 (D30) and 90 (D90) among patients with systemic lupus erythematosus (SLE) in France. Conversely, they noted that an unchanged survival rate of patients with SLE with COVID-19-AOF will require hospitalization compared with patients without SLE COVID-19-AOF at D90. This study is a valuable addition to the literature. However, we share some concerns about this article to the authors.
  First, the selection bias may be suspect in this study. A selection bias occurs when those in charge of the recruitment or enrollment of patients (recruiters) selectively enroll patients into the study based on what the next observation allocation is likely to be.2 At D30, 43 (21.9%) in-hospital deaths were recorded among patients with SLE with COVID-19-AOF compared with 31,274 (27.6%) in the unmatched patients without SLE with COVID-19-AOF. At baseline (D30), they may enroll a sick patient in patients with SLE with COVID-19-AOF compared with patients without SLE with COVID-19-AOF. This strategy can lead to substantially biased estimates of the survival of patients with COVID-19-AOF between D30 and D90 and misleading conclusions.
  Second, prior studies have shown numerous AOFs, and disease severity of COVID-19 is independently associated with the increased risk of mortality.3,4 Furthermore, several parameters may predict disease severity and overall survival for COVID-19. For example, Acute Physiology and Chronic Health Evaluation II score is a classification tool used to measure disease severity and predict an individual’s risk of mortality in a hospital.5 Hence, the number of AOF and disease severity are clinically important risk factors. However, the baseline characteristics between the two groups were not defined in this study. As the number of AOF and disease severity of COVID-19 between the two groups was not available in this study, residual confounding bias may occur because of unmeasured factors.
  Although we have some concerns regarding the study by Mageau et al.,1 we applaud the authors for their commendable work and hope that this study will benefit readers. We look forward to further work on the important topic of the predictive factors of survival after COVID-19-AOF among inpatients with SLE and hope that early preventive application for mortality will benefit patients with SLE with COVID-19-AOF.

  References:
  1. Mageau A, Papo T, Ruckly S, et al. Survival after COVID-19-associated organ failure among inpatients with systemic lupus erythematosus in France: a nationwide study. Ann Rheum Dis 2022;81:569-74.
  2. Neyens T. Did an effect of kidney transplantation on COVID-19 mortality go unnoticed due to selection bias? Transpl Int 2021;34:773-5.
  3. Meijs DAM, van Bussel BCT, Stessel B, et al. Better COVID-19 intensive care unit survival in females, independent of age, disease severity, comorbidities, and treatment. Sci Rep 2022:12:734.
  4. Del Valle MD, Kim-Schulze S, Huang HH, et al. An inflammatory cytokine signature predicts COVID-19 severity and survival. Nat Med 2020;26:1636–43.
  5. Zou X, Li S, Fang M, et al. Acute Physiology and Chronic Health Evaluation II Score as a Predictor of Hospital Mortality in Patients of Coronavirus Disease 2019. Crit Care Med 2020;48:e657–65.

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  Conflict of Interest:
  None declared.

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