Allogeneic hematopoietic cell transplantation after infection with SARS-CoV-2 during the COVID-19 pandemic: a multicenter retrospective analysis

To the Editor:

At the onset of the COVID-19 pandemic, transplanters faced the unprecedented challenge of balancing the unknown risks of a SARS-CoV-2 infection in patients requiring allogeneic haematopoietic stem cell transplantation (alloHCT) against the benefits of this curative procedure. While alloHCT remains a cornerstone therapy for haematological malignancies, its significant risk of non-relapse mortality (NRM) and prolonged susceptibility to infections make careful timing critical, particularly in the context of modifiable risk factors such as infections [1, 2].

A previous study involving seven patients highlighted the uncertainty early during the pandemic: here transplanters had adopted precautionary measures such as treating patients in insulated areas with dedicated teams [3]. To assess the impact of pre-transplant SARS-CoV-2 infection on alloHCT outcomes, we conducted a retrospective, multicentre study involving 75 patients from 16 centers in Germany and Austria. Patients were categorized into COVID-19 disease severity groups based on WHO criteria. All patients had tested negative for SARS-CoV-2 at the start of conditioning. Severe and critical COVID-19 severity were combined into one group. There were no exclusion criteria.

The study was approved by the local ethics committee of the Eberhard Karls University Tübingen on 26th of May 2021 (project number: 302/2021B02).

Of the 75 patients included, 31 had mild, 6 moderate, and 12 severe/ critical COVID-19. COVID-19 classification of 26 patients remained unknown. The median time from diagnosis of neoplasia to COVID-19 varied between severity groups: 109 days for mild, 374 days for moderate, and 17 days for severe/ critical infections. The median FEV1 prior to alloHCT was 91% in mild and moderate cases, compared to 74% in severe/ critical cases.

The cumulative incidences of relapse and NRM at 365 days for all patients were 17.31% (95% CI: 6.24–28.38) and 8.32% (95% CI: 1.15–15.49), respectively. According to COVID-19 severity, relapse rates were 32.1% for mild, 0% for moderate, and 27.98% for severe/ critical cases, while NRM rates were 0%, 33.33%, and 19.64%, respectively. NRM differences were statistically significant (p = 0.03).

Survival analysis revealed significant differences between severity groups. Patients with mild COVID-19 had the highest 365-day survival (90.9%, 95%CI: 79.5–100%), followed by moderate (66.7%, 95% CI: 37.9–100%) and severe/ critical cases (51.1%, 95% CI: 27.9–93.6%). The difference in overall survival (OS) was statistically significant (p = 0.025).

When stratifying OS by both COVID-19 severity and Karnofsky Index, patients with mild disease and a high Karnofsky Index (90–100) had the best outcomes (94.4% survival at 365 days). Conversely, patients with severe/ critical COVID-19 and a low Karnofsky Index (<90) had the worst outcomes (51.4% survival at 365 days). Although the combined effect of COVID-19 severity and Karnofsky Index on OS was not statistically significant (p = 0.12), these results emphasize the importance of functional assessment in alloHCT candidates.

Univariate Cox regression analysis (Table 1) identified three significant predictors of outcome. First, a high Karnofsky Index (90–100) was associated with significantly better disease-free survival (DFS) compared to a Karnofsky Index <90 (HR: 0.23, 95% CI: 0.07–0.78, p = 0.019). Second, patients with severe/ critical COVID-19 had a higher hazard ratio for death compared to those with mild disease (HR: 7.20, 95% CI: 1.39–37.2, p = 0.019). Third, a higher FEV1/FVC ratio before alloHCT was associated with a slightly increased hazard for OS and DFS (HR: 1.01, p = 0.049 and p = 0.028, respectively).

Table 1 Univariate cox regression analysis of patient and COVID-19 characteristics on OS and DFS.
Full size table

Our study highlights the pivotal role of COVID-19 severity in determining post-transplant outcomes. Patients with mild COVID-19 demonstrated significantly better OS and lower NRM rates compared to those with severe/ critical disease. These results are consistent with previous reports that severe/ critical COVID-19 exacerbates underlying health conditions, leading to worse prognoses in immunocompromised patients [4,5,6].

Consistent with prior studies, no significant association between COVID-19 severity and the incidence of Graft-versus-Host Disease (GvHD) was found [3, 7]. The Karnofsky Index emerged as a key independent predictor of survival. Although the combined effect of the Karnofsky Index and COVID-19 severity on survival showed a trend toward association, it did not reach statistical significance. These findings highlight the critical role of functional status assessment in pre-transplant risk stratification.

The evolving impact of improved pandemic management strategies is also evident in our results. By 2022, severe COVID-19 cases were absent from our cohort, likely reflecting the benefits of vaccination, antiviral therapies, and improved infection control measures. These findings highlight the adaptability of transplant practices during this pandemic. They might provide a framework for managing similar crises in the future.

The results of our study should be interpreted with caution due to limitations inherent to the retrospective design. The small sample size and missing data, particularly regarding COVID-19 severity and duration, limit the generalizability of our results. Not all patients were treated for COVID-19 at the participating centers, limiting the availability of consistent data. Future research involving larger cohorts and standardized data collection is needed to validate our findings and explore the mechanisms underlying the observed associations.

In conclusion, our study underscores the profound influence of COVID-19 severity and pre-transplant functional status on alloHCT outcomes. We advocate for continued prioritization of preventive measures, including vaccination and tailored pre-transplant assessments, to optimize patient outcomes in this vulnerable population.

Related Articles

Effector CD8 T cell differentiation in primary and breakthrough SARS-CoV-2 infection in mice

The nature of the effector and memory T cell response in the lungs following acute SARS-CoV-2 infections remains largely unknown. To define the pulmonary T-cell response to COVID-19, we compared effector and memory T-cell responses to SARS-CoV-2 and influenza A virus (IAV) in mice. Both viruses elicited potent effector T cell responses in lungs, but memory T cells showed exaggerated contraction in SARS-CoV-2-infected mice. Specifically, unlike the T-bet/EOMES-driven effector transcription program in IAV lungs, SARS-CoV-2-specific CD8 T cells embarked on a STAT-3-centric transcriptional program, a defining characteristic of a pro-fibro-inflammatory program: limited cytotoxicity, diminished expression of tissue-protective inhibitory receptors (PD-1, LAG-3, and TIGIT), and augmented mucosal imprinting (CD103). Circulating CD45RO+HLA-DR+ CD8 T cells in hospitalized COVID-19 patients expressed elevated levels of STAT-3 and low levels of TIGIT. IL-6 blockade experiments implicated IL-6 in STAT-3 induction and downregulation of PD-1 expression on SARS-CoV-2-specific primary effector CD8 T cells. Memory CD8 T cells specific to a single epitope, induced by mucosal vaccination, differentiated into cytotoxic effectors and expressed high levels of CD103, effectively reducing viral burden in lungs following a breakthrough SARS-CoV-2 infection. Our findings have implications for developing targeted immunotherapies to mitigate immunopathology and promote protective T cell immunity to SARS-CoV-2.

Potent and broadly neutralizing antibodies against sarbecoviruses elicited by single ancestral SARS-CoV-2 infection

The emergence of various SARS-CoV-2 variants presents challenges for antibody therapeutics, emphasizing the need for more potent and broadly neutralizing antibodies. Here, we employed an unbiased screening approach and successfully isolated two antibodies from individuals with only exposure to ancestral SARS-CoV-2. One of these antibodies, CYFN1006-1, exhibited robust cross-neutralization against a spectrum of SARS-CoV-2 variants, including the latest KP.2, KP.3 and XEC, with consistent IC50 values ranging from ~1 to 5 ng/mL. It also displayed broad neutralization activity against SARS-CoV and related sarbecoviruses. Structural analysis revealed that these antibodies target shared hotspot but mutation-resistant epitopes, with their Fabs locking receptor binding domains (RBDs) in the “down” conformation through interactions with adjacent Fabs and RBDs, and cross-linking Spike trimers into di-trimers. In vivo studies conducted in a JN.1-infected hamster model validated the protective efficacy of CYFN1006-1. These findings suggest that antibodies with cross-neutralization activities can be identified from individuals with exclusively ancestral virus exposure.

IL-1β drives SARS-CoV-2-induced disease independently of the inflammasome and pyroptosis signalling

Excessive inflammation and cytokine release are hallmarks of severe COVID-19. Certain programmed cell death processes can drive inflammation, however, their role in the pathogenesis of severe COVID-19 is unclear. Pyroptosis is a pro-inflammatory form of regulated cell death initiated by inflammasomes and executed by the pore-forming protein gasdermin D (GSDMD). Using an established mouse adapted SARS-CoV-2 virus and a panel of gene-targeted mice we found that deletion of the inflammasome (NLRP1/3 and the adaptor ASC) and pore forming proteins involved in pyroptosis (GSDMA/C/D/E) only marginally reduced IL-1β levels and did not impact disease outcome or viral loads. Furthermore, we found that SARS-CoV-2 infection did not trigger GSDMD activation in mouse lungs. Finally, we did not observe any difference between WT animals and mice with compound deficiencies in the pro-inflammatory initiator caspases (C1/11/12−/−). This indicates that the classical canonical and non-canonical pro-inflammatory caspases known to process and activate pro-IL-1β, pro-IL-18 and GSDMD do not substantially contribute to SARS-CoV-2 pathogenesis. However, the loss of IL-1β, but not the absence of IL-18, ameliorated disease and enhanced survival in SARS-CoV-2 infected animals compared to wildtype mice. Collectively, these findings demonstrate that IL-1β is an important factor contributing to severe SARS-CoV-2 disease, but its release was largely independent of inflammasome and pyroptotic pathways.

The comprehensive SARS-CoV-2 ‘hijackome’ knowledge base

The continuous evolution of SARS-CoV-2 has led to the emergence of several variants of concern (VOCs) that significantly affect global health. This study aims to investigate how these VOCs affect host cells at proteome level to better understand the mechanisms of disease. To achieve this, we first analyzed the (phospho)proteome changes of host cells infected with Alpha, Beta, Delta, and Omicron BA.1 and BA.5 variants over time frames extending from 1 to 36 h post infection. Our results revealed distinct temporal patterns of protein expression across the VOCs, with notable differences in the (phospho)proteome dynamics that suggest variant-specific adaptations. Specifically, we observed enhanced expression and activation of key components within crucial cellular pathways such as the RHO GTPase cycle, RNA splicing, and endoplasmic reticulum-associated degradation (ERAD)-related processes. We further utilized proximity biotinylation mass spectrometry (BioID-MS) to investigate how specific mutation of these VOCs influence viral–host protein interactions. Our comprehensive interactomics dataset uncovers distinct interaction profiles for each variant, illustrating how specific mutations can change viral protein functionality. Overall, our extensive analysis provides a detailed proteomic profile of host cells for each variant, offering valuable insights into how specific mutations may influence viral protein functionality and impact therapeutic target identification. These insights are crucial for the potential use and design of new antiviral substances, aiming to enhance the efficacy of treatments against evolving SARS-CoV-2 variants.

Distinct airway epithelial immune responses after infection with SARS-CoV-2 compared to H1N1

Children are less likely than adults to suffer severe symptoms when infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), while influenza A H1N1 severity is comparable across ages except for the very young or elderly. Airway epithelial cells play a vital role in the early defence against viruses via their barrier and immune functions. We investigated viral replication and immune responses in SARS-CoV-2-infected bronchial epithelial cells from healthy paediatric (n = 6; 2.5–5.6 years old) and adult (n = 4; 47–63 years old) subjects and compared cellular responses following infection with SARS-CoV-2 or Influenza A H1N1. While infection with either virus triggered robust transcriptional interferon responses, including induction of type I (IFNB1) and type III (IFNL1) interferons, markedly lower levels of interferons and inflammatory proteins (IL-6, IL-8) were released following SARS-CoV-2 compared to H1N1 infection. Only H1N1 infection caused disruption of the epithelial layer. Interestingly, H1N1 infection resulted in sustained upregulation of SARS-CoV-2 entry factors FURIN and NRP1. We did not find any differences in the epithelial response to SARS-CoV-2 infection between paediatric and adult cells. Overall, SARS-CoV-2 had diminished potential to replicate, affect morphology and evoke immune responses in bronchial epithelial cells compared to H1N1.

Responses

Your email address will not be published. Required fields are marked *