# The mortality of COVID-19 in CML patients from 2020 until 2022: results from the EPICOVIDEHA survey

Shaimaa El-Ashwah, Jon Salmanton-García, Yavuz M. Bilgin, Federico Itri, Pavel Žák, Barbora Weinbergerová, Luisa Verga, Ali S. Omrani, Maria Gomes Da Silva, Tomáš Szotkowski, et al.

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Shaimaa El-Ashwah, Jon Salmanton-García, Yavuz M. Bilgin, Federico Itri, Pavel Žák, et al. The mortality of COVID-19 in CML patients from 2020 until 2022: results from the EPICOVIDEHA survey. Leukemia & lymphoma, 2023, 10.1080/10428194.2023.2280886. hal-04342434

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# The mortality of COVID-19 in CML patients from 2020 until 2022: results from the EPICOVIDEHA survey

Shaimaa El-Ashwah, Jon Salmanton-García, Yavuz M. Bilgin, Federico Itri, Pavel Žák, Barbora Weinbergerová, Luisa Verga, Ali S. Omrani, Maria Gomes da Silva, Tomáš Szotkowski, Monia Marchetti, Caterina Buquicchio, Marcio Nucci, Martin Schönlein, Francesca Farina, Caroline Besson, Lucia Prezioso, Summiya Nizamuddin, Julio Dávila-Valls, Sonia Martín-Pérez, Valentina Bonuomo, Jaap Van Doesum, Maria Chiara Tisi, Francesco Passamonti, Gustavo-Adolfo Méndez, Stef Meers, Johan Maertens, Alberto López-García, Andreas Glenthøj, Matteo Bonnani, Ikhwan Rinaldi, Irati Ormazabal-Vélez, Jorge Labrador, Austin Kulasekararaj, Ildefonso Espigado, Fatih Demirkan, Nick De Jonge, Graham P. Collins, Maria Calbacho, Ola Blennow, Murtadha Al-Khabori, Tatjana Adžić-Vukičević, Elena Arellano, Bojana Mišković, Miloš Mladenović, Anna Nordlander, Zdeněk Ráčil, Emanuele Ammatuna, Raul Cordoba, Ditte Stampe Hersby, Stefanie Gräfe, Ziad Emarah, Michaela Hanakova, Maria Vittoria Sacchi, Marriyam Ijaz, Laman Rahimli, Raquel Nunes Rodrigues, Giovanni Paolo Maria Zambrotta, Francesco Marchesi, Oliver A. Cornely & Livio Pagano

**To cite this article:** Shaimaa El-Ashwah, Jon Salmanton-García, Yavuz M. Bilgin, Federico Itri, Pavel Žák, Barbora Weinbergerová, Luisa Verga, Ali S. Omrani, Maria Gomes da Silva, Tomáš Szotkowski, Monia Marchetti, Caterina Buquicchio, Marcio Nucci, Martin Schönlein, Francesca Farina, Caroline Besson, Lucia Prezioso, Summiya Nizamuddin, Julio Dávila-Valls, Sonia Martín-Pérez, Valentina Bonuomo, Jaap Van Doesum, Maria Chiara Tisi, Francesco Passamonti, Gustavo-Adolfo Méndez, Stef Meers, Johan Maertens, Alberto López-García, Andreas Glenthøj, Matteo Bonnani, Ikhwan Rinaldi, Irati Ormazabal-Vélez, Jorge Labrador, Austin Kulasekararaj, Ildefonso Espigado, Fatih Demirkan, Nick De Jonge, Graham P. Collins, Maria Calbacho, Ola Blennow, Murtadha Al-Khabori, Tatjana Adžić-Vukičević, Elena Arellano, Bojana Mišković, Miloš Mladenović, Anna Nordlander, Zdeněk Ráčil, Emanuele Ammatuna, Raul Cordoba, Ditte Stampe Hersby, Stefanie Gräfe, Ziad Emarah, Michaela Hanakova, Maria Vittoria Sacchi, Marriyam Ijaz, Laman Rahimli, Raquel Nunes Rodrigues, Giovanni Paolo Maria Zambrotta, Francesco Marchesi, Oliver A. Cornely & Livio Pagano (15 Nov 2023): The mortality of COVID-19 in CML patients from 2020 until 2022: results from the EPICOVIDEHA survey, Leukemia & Lymphoma, DOI: 10.1080/10428194.2023.2280886

**To link to this article:** https://doi.org/10.1080/10428194.2023.2280886

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# The mortality of COVID-19 in CML patients from 2020 until 2022: results from the EPICOVIDEHA survey

Shaimaa El-Ashwah* ID, Jon Salmanton-García b,c* ID, Yavuz M. Bilgin d* ID, Federico Itri e ID, Pavel Žák f ID, Barbora Weinbergerová g ID, Luisa Verga h,i ID, Ali S. Omrani j ID, Maria Gomes da Silva k ID, Tomáš Szotkowski l, Monia Marchetti m ID, Caterina Buquicchio n ID, Marcio Nucci o ID, Martin Schönlein p ID, Francesca Farina q ID, Caroline Besson r,s ID, Lucia Prezioso t ID, Summiya Nizamuddin u, Julio Dávila-Valls v ID, Sonia Martín-Pérez v ID, Valentina Bonuomo w,x ID, Jaap Van Doesum y ID, Maria Chiara Tisi z ID, Francesco Passamonti aa ID, Gustavo-Adolfo Méndez ab ID, Stef Meers ac ID, Johan Maertens ad,ae ID, Alberto López-García af ID, Andreas Glenthøjag ID, Matteo Bonnani ah ID, Ikhwani Rinaldi ai, Irati Ormazabal-Vélez aj ID, Jorge Labrador ak ID, Austin Kulasekararajal ID, Ildefonso Espigado am ID, Fatih Demirkan an ID, Nick De Jonge ao ID, Graham P. Collins ap, Maria Calbacho aq ID, Ola Blennow ar ID, Murtadha Al-Khabori as ID, Tatjana Adžić-Vukičević at, Elena Arellano am, Bojana Mišković at,au, Miloš Mladenović at,au ID, Anna Nordlander ar, Zdeněk Ráčilav ID, Emanuele Ammatuna v ID, Raul Cordoba aw ID, Ditte Stampe Hersby ax ID, Stefanie Gräfe b,c,ay,az ID, Ziad Emarahb a ID, Michaela Hanakova av, Maria Vittoria Sacchi m ID, Marriyam Ijaz bb, Laman Rahimli b,c ID, Raquel Nunes Rodrigues k ID, Giovanni Paolo Maria Zambrotta i,b,c ID, Francesco Marchesi bd ID, Oliver A. Cornely b,c,be,bf,bg t ID and Livio Pagano ah,bh t ID

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<footnote>*Oncology Center, Mansoura University, Mansoura, Egypt; †Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, University Hospital Cologne, Institute of Translational Research, Cologne, Germany; ‡Department I of Internal Medicine, Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf (CIO ABCD) and Excellence Center for Medical Mycology (ECMM), University of Cologne, University Hospital Cologne, Cologne, Germany; §Department of Internal Medicine, ADRZ, Goes, Netherlands; €San Luigi Gonzaga Hospital – Orbassano, Orbassano, Italy; †University Hospital Hradec Králové, Hradec Králové, Czech Republic; gDepartment of Internal Medicine – Hematology and Oncology, Masaryk University Hospital Brno, Brno, Czech Republic; hAzienda Ospedaliera San Gerardo – Monza, Monza, Italy; iUniversità Milano-Bicocca, Milan, Italy; jCommunicable Disease Center, Hamad Medical Corporation, Doha, Qatar; kPortuguese Institute of Oncology, Lisbon, Portugal; lUniversity Hospital Olomouc, Olomouc, Czech Republic; mAzienda Ospedaliera Nazionale SS. Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; nEmatologia con Trapianto, Ospedale Dimiccoli Barletta, Barletta, Italy; oFederal University of Rio de Janeiro, Rio de Janeiro, Brazil; pDepartment of Oncology, Hematology and Bone Marrow Transplantation with Section of Pneumology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany; qIRCCS Ospedale San Raffaele, Milan, Italy; rCentre Hospitalier de Versailles, Le Chesnay, France; sUniversité Paris-Saclay, UVSQ, Inserm, Équipe "Exposome et Hérédité", CESP, Villejuif, France; tHospital University of Parma – Hematology and Bone Marrow Unit, Parma, Italy; uMemorial Cancer Hospital and Research Centre, Lahore, Pakistan; vHospital Nuestra Señora de Sonsoles, Ávila, Spain; wDepartment of Medicine, Section of Hematology, University of Verona, Verona, Italy; xDepartment of Clinical and Biological Sciences, University of Turin, Turin, Italy; yUniversity Medical Center Groningen, Groningen, Netherlands; zOspedale San Bortolo, Vicenza, Italy; aaDepartment of Medicine and Surgery, University of Insubria and ASST Sette Laghi, Ospedale di Circolo di Varese, Varese, Italy; abHospital Escuela de Agudos Dr. Ramón Madariaga, Posadas, Argentina; acAZ KLINA, Brasschaat, Belgium; adDepartment of Microbiology, Immunology, and Transplantation, KULeuven, Leuven, Belgium; aeDepartment of Hematology, UZ Leuven, Leuven, Belgium; afFundacion Jimenez Diaz University Hospital, Health Research Institute IIS-FJD, Madrid, Spain; agDepartment of Hematology, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark; ahHematology Unit, Fondazione Policlinico Universitario Agostino Gemelli – IRCCS, Rome, Italy; aiDivision of Hematology and Medical Oncology, Department of Internal Medicine, Universitas Indonesia – Cipto Mangunkusumo Hospital, Jakarta, Indonesia; ajComplejo Hospitalario de Navarra, Iruña-Pamplona, Spain; akDepartment of Hematology, Research Unit, Hospital Universitario de Burgos, Burgos, Spain; alKing’s College Hospital, London, UK; amDepartment of Hematology, University Hospital Virgen Macarena – University Hospital Virgen del Rocío, Instituto de Biomedicina de Sevilla (IBIS/CSIC), Universidad de Sevilla (Departamento de Medicina), Seville, Spain; anDivision of Hematology, Dokuhl University, Izmir, Turkey; aoAmsterdam UMC, Location VUmc, Amsterdam, Netherlands; apNIHR Oxford Biomedical Research Centre, Churchill Hospital, Oxford, UK; aqHospital Universitario 12 de Octubre, Madrid, Spain; arDepartment of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden; asSultan Qaboos University Hospital, Muscat, Oman; atCOVID-19 Hospital "Batajnica", Belgrade, Serbia; auClinic for Orthopedic Surgery and Traumatology, University Clinical Center of Serbia, Belgrade, Serbia; avInstitute of Hematology and Blood Transfusion, Prague, Czech Republic; awI. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany; axIII. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany; ayShaukat Khanum Memorial Cancer Hospital and Research Centre, Lahore, Pakistan; azHematology and Stem Cell Transplant Unit, IRCCS Regina Elena</footnote>
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National Cancer Institute, Rome, Italy; baClinical Trials Centre Cologne (ZKS Köln), University of Cologne, University Hospital Cologne, Cologne, Germany; bbCenter for Molecular Medicine Cologne (CMMC), University of Cologne, Faculty of Medicine, and University Hospital Cologne, Cologne, Germany; bcGerman Centre for Infection Research (DZIF), Partner Site Bonn-Cologne, Cologne, Germany; bdHematology Unit, Università Cattolica del Sacro Cuore, Rome, Italy

## ABSTRACT

Since the beginning of the COVID-19 pandemic, there has been an overall improvement in patient mortality. However, haematological malignancy patients continue to experience significant impacts from COVID-19, including high rates of hospitalization, intensive care unit (ICU) admissions, and mortality. In comparison to other haematological malignancy patients, individuals with chronic myeloid leukemia (CML) generally have better prognosis. This study, conducted using a large haematological malignancy patient database (EPICOVIDEHA), demonstrated that the majority of CML patients experienced mild infections. The decline in severe and critical infections over the years can largely be attributed to the widespread administration of vaccinations and the positive response they elicited. Notably, the mortality rate among CML patients was low and exhibited a downward trend in subsequent years. Importantly, our analysis provided confirmation of the effectiveness of vaccinations in CML patients.

## ARTICLE HISTORY

Received 20 July 2023

Revised 21 September 2023

Accepted 10 October 2023

## KEYWORDS

Chronic myeloid leukemia; tirosine kinase inhibitor; COVID-19; SARS-CoV-2; neoplasia; vaccines

## Introduction

Chronic myeloid leukemia (CML) is a rare myeloproliferative neoplasm that affects approximately 1–2 individuals per 100,000 adults. It is characterized by the presence of BCR-ABL1 protein resulting from the fusion of the BCR gene on chromosome 22 and the ABL1 gene on chromosome 9 [1]. Following the introduction of tyrosine kinase inhibitors (TKIs) as a treatment for CML, there have been substantial changes in therapeutic options. This advancement has led to a remarkable improvement in overall survival rates, increasing from 20% to 90% [2,3]. As a result, the life expectancy of CML patients has now become comparable to that of the general population across all age groups [4]. Generally, TKIs are well tolerated [5]. However, during the initial months of TKIs treatment, some patients may experience grade 3–4 neutropenia, with a toxicity incidence of 14%–17% [6]. Infections, primarily viral, can occur in around 14% of patients treated with imatinib, while the incidence varies between 1 and 8% with second-generation TKIs [6].

The emergence of coronavirus disease 2019 (COVID-19) in December 2019 led to a global pandemic with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) acquiring multiple mutations, resulting in variants of concern such as Alpha, Beta, Gamma, Delta, and Omicron [7,8]. TKIs have demonstrated antiviral efficacy against coronaviruses in vitro. However, some TKIs may produce effects similar to those caused by COVID-19 [9]. The mortality for patients with high-risk hematologic malignancies has ranged from 14% to 34% [10–12]. With the introduction of COVID-19 vaccinations in subsequent years, the overall mortality rate has decreased. However, among

patients with haematological malignancy, the mortality rate remains higher compared to other malignancies [13]. Despite this, CML patients with COVID-19 generally have better prognosis compared to those with other hematologic malignancies [10].

The primary objective of this study is to evaluate the mortality of CML patients with COVID-19 during the years 2020, 2021, and 2022. Additionally, the study examines the COVID-19 vaccination rate and its impact on mortality and other prognostic factors in CML patients.

## Methods

In February 2020, the EPICOVIDEHA was established as an international cooperative registry by the European Hematology Association (EHA) Specialized Working Group ‘Infection in Hematology’. The multicenter, non-interventional study (Study ID: 3226) received approval from the local Institutional Review Board and Ethics Committee of the Fondazione Policlinico Universitario Agostino Gemelli—IRCCS, Università Cattolica del Sacro Cuore in Rome, Italy. Additionally, the EPICOVIDEHA project may require authorization from the local ethics committee of each participating institution. The registration number for EPICOVIDEHA on ClinicalTrials.gov is NCT 04733729 (http://www.clinicaltrials.gov).

Researchers from any location were invited to report any instances of COVID-19 recorded in patients with haematological malignancies at their respective institutions since the onset of the pandemic. The electronic case report form was accessible online at www.clinicalsurveys.net (EFS Summer 2021, TIVIAN GmbH,
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Cologne, Germany). Participating institutions could contribute anonymized clinical data through a survey covering various topics, including identification, demographics, underlying conditions, hematological malignancy, COVID-19, and mortality. Cases meeting the following inclusion criteria were eligible for registration: (1) age 18 or older, (2) a history of active hematological malignancy at any stage within the five years preceding COVID-19, and (3) confirmation of SARS-CoV-2 infection through real-time reverse transcriptase polymerase chain reaction (RT-PCR) diagnostic panels or antigen test kits.

COVID-19 severity was set as follows: asymptomatic (absence of clinical signs or symptoms); mild (non-pneumonia and mild pneumonia); severe (characterized by dyspnea, respiratory rate ≥30 breaths per minute, SpO2 ≤93%, PaO2/FiO2 <300, or lung infiltrates >50%); and critical, primarily encompassing patients requiring intensive care (experiencing respiratory failure, septic shock, or multiple organ dysfunction or failure) (which also encompassed critical cases).

Qualitative demographic and clinical data were described using frequencies and percentages, while quantitative variables were summarized using medians and interquartile ranges (IQR). Appropriate statistical tests such as the Chi-squared test, Fisher's exact test, and Mann-Whitney U test were employed for making comparisons. The use of Cox multivariable regressions allowed for the identification of predictors of mortality. The statistical analysis was performed using SPSS software (version 25.0, Chicago, IL, United States).

## Results

From February 2020 to September 2022, a total of 231 CML patients with COVID-19 were enrolled in the EPICOVIDEHA registry. Among them, males accounted for 55.8% (n=129) of the entire cohort. The median age at the time of infection was 56 years, with an IQR of 21–90 and a range of 44–70. Out of all the patients, 56 (24.2%) had received a vaccination before contracting COVID-19. Specifically, in 2021, 21 out of 43 patients (48.8%) had been vaccinated, while in 2022, 35 out of 46 patients (76.1%). In terms of SARS-CoV-2 variants, 6 patients (2.6%) were infected with the Wild type, 2 patients (0.9%) with the Delta variant, and 26 patients (11.3%) with the Omicron variant. In 2022, the Omicron variant was the only documented variant and affected 20 patients (43.5%). As for the severity of infection, 50 patients (21.6%) experienced asymptomatic SARS-CoV-2 infection, while 99 patients (42.9%) had a mild infection. Severe and critical infections were observed in a total of 82 patients (35.5%). The rate of severe and critical infections significantly decreased over time, with 61/142 patients (43%) in 2020, 13/43 patients (30.3%) in 2021, and 8/46 patients (17.4%) in 2022. During the course of COVID-19, CML patients were monitored for haematological grade 3-4 TKIs-related adverse events, which revealed a prevalence of 3% for anemia (n=7), 2.2% for neutropenia (n=5), 1.7% for thrombocytopenia (n=4), 0.9% for thrombosis (n=2), and 0.9% for hemorrhage (n=2). Non-haematological TKIs-related adverse events

<figure><img src="image_14.png" /><figcaption>**Figure 1.** Overall survival for vaccinated vs not vaccinated.</figcaption></figure>
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included 2.2% pulmonary events (n=5), 1.7% musculoskeletal events (n=4), 1.3% gastrointestinal events (n=3), 0.4% hepatotoxic events, and non-viral infections (n=1). Out of all the patients, 96 (41.6%) were admitted to the hospital, with a median stay duration of 13 d, with an IQR of 6.5-21.5 and a range of 1-130. The rate of hospital admission was significantly higher in 2020 compared to 2021 and 2022 (p=.004). Additionally, 16 CML patients were admitted to the intensive care unit (ICU) for a median duration of 12 d, with 13 patients (9.2%) in 2020 and 3 patients (7%) in 2021 (Tables 1 and 2).

The study examined the overall survival rate, revealing that 92.2% (213/231) of individuals were alive at the end of the follow-up period. Significant variations were observed in the distribution of patients based on their age, with a median age of 55 among those who survived, compared to 72 among those who did not (p=.005). The presence of comorbidities at the onset of COVID-19 also had a notable impact on mortality. Patients without comorbidities had a higher survival rate (n=115, 54.0%) compared to those with comorbidities, which ranged from 8.5% (n=18) to 24.9% (n=53, p=.005). Chronic cardiopathy and diabetes mellitus were particularly concerning, with the latter significantly affecting survival (p=.007). The history of malignancy treatment also exhibited significant differences. Patients who received drug-based therapies had an 86.1% (n=199) survival rate. However, the specific type of treatment played a crucial role, with first-generation TKIs like imatinib showing better survival rates compared to other TKIs. Furthermore, patients treated within the last month before the onset of COVID-19 had a higher survival rate (n=158, 68.4%) compared to those treated further in the past. Survival rates among patients also varied based on their malignancy status at the onset of COVID-19. Patients with controlled malignancy had a higher survival rate (n=165, 77.5%) compared to those with active malignancy (n=22, 10.3%) or stable malignancy (n=23, 10.8%). Regarding vaccination status, there were noticeable trends, with vaccinated patients showing a lower mortality rate (n=1, 5.6%) compared to those who were not vaccinated (n=17, 94.4%), although the difference did not reach statistical significance (p=.081). More specifically, Six patients had received just one vaccine dose, and all of them successfully recovered (100%). In the group that received two vaccine doses, consisting of 16 patients, only one patient did not survive (93.75% survival rate). On the other hand, among the 32 patients who received three vaccine doses, all of them made a full recovery (100% survival rate). Additionally, one patient who had

received four vaccine doses also emerged as a survivor in our study (100% survival rate) (Figure 1). Across the study duration, the hospital admission rate stood at 41.5% (n=96), with 36.6% (n=78) among surviving patients and a full 100.0% (n=18) among deceased patients (p<.001, Tables 1 and 2).

The univariable Cox regression model revealed that older age, baseline active malignancy, baseline cardiopathy, diabetes mellitus, liver disease, COVID-19 diagnosis via screening, and admission in the ICU unit were associated with a higher mortality. In the multivariable Cox regression analysis, however, age-stable malignancy at COVID-19, and ICU admission (Table 3).

There was no significant difference in overall survival probability across years (Figure 2).

## Discussion

The data presented in this study indicate that CML patients predominantly experienced mild infections. The rates of severe and critical infections, as well as hospital and ICU admissions, were higher in 2020 compared to 2021 and 2022. Furthermore, the mortality rate was higher in 2020 and among unvaccinated patients. Multivariable analysis identified age, CML disease status, and ICU admission as significant independent predictors of mortality.

Following the onset of the COVID-19 outbreak, a study conducted in Hubei, China, focused on 530 CML outpatients who completed questionnaires, revealing a low prevalence of COVID-19 (0.9%) [14]. This observation was corroborated by other studies, which also demonstrated a mild course of COVID-19 in CML patients [15-17]. In the current study, it was found that 21.6% of patients had asymptomatic COVID-19, while 42.9% experienced a mild infection. Severe and critical infections were confirmed in approximately one-third of patients (35.5%). These findings are consistent with previous studies involving smaller numbers of CML patients [17-19].

During the initial year of the pandemic, a total of 3,801 patients were analyzed by EPICOVIDEHA, revealing an overall mortality rate of 31% [20]. In the present analysis, which included 231 CML patients, the mortality rate was approximately 8%. A study focusing on 217 CML patients with COVID-19 reported a mortality rate of 5.5% during the first year of the pandemic [21]. In other studies, with smaller patient populations, the mortality rates ranged between 6.3% and 11.1% [16,17,19]. Notably, the incidence of mortality among CML patients was lower compared to other hematologic malignancies, suggesting a potential protective
<figure><img src="image_16.png" /><figcaption>Table 1. Demographic, clinical characteristics, and summary of received treatments for CML at the time of COVID-19 diagnosis.</figcaption></figure>

<table><thead><tr><th rowspan="2"></th><th colspan="2">Overall</th><th colspan="2">Alive</th><th colspan="2">Dead</th><th rowspan="2">p value</th></tr><tr><th>n</th><th>%</th><th>n</th><th>%</th><th>n</th><th>%</th></tr></thead><tbody><tr><td></td><td>231</td><td>100.0</td><td>213</td><td>92.2</td><td>18</td><td>7.8</td><td></td></tr><tr><td><strong>Sex</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Female</td><td>102</td><td>44.2</td><td>94</td><td>44.1</td><td>8</td><td>44.4</td><td>0.980</td></tr><tr><td>Male</td><td>129</td><td>55.8</td><td>119</td><td>55.9</td><td>10</td><td>55.6</td><td></td></tr><tr><td><strong>Age</strong></td><td>56 (44-70) [21-90]</td><td></td><td>55 (43-67) [21-90]</td><td></td><td>72 (59-82) [29-90]</td><td></td><td><strong>0.005</strong></td></tr><tr><td><strong>Comorbidities at COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>No comorbidities</td><td>118</td><td>51.1</td><td>115</td><td>54.0</td><td>3</td><td>16.7</td><td><strong>0.005</strong></td></tr><tr><td>1 comorbidity</td><td>59</td><td>25.5</td><td>53</td><td>24.9</td><td>6</td><td>33.3</td><td></td></tr><tr><td>2 comorbidities</td><td>32</td><td>13.9</td><td>27</td><td>12.7</td><td>5</td><td>27.8</td><td></td></tr><tr><td>3 or more comorbidities</td><td>22</td><td>9.5</td><td>18</td><td>8.5</td><td>4</td><td>22.2</td><td></td></tr><tr><td>Chronic cardiopathy</td><td>58</td><td>25.1</td><td>48</td><td>22.5</td><td>10</td><td>55.6</td><td><strong>0.004</strong></td></tr><tr><td>Chronic pulmonary disease</td><td>21</td><td>9.1</td><td>18</td><td>8.5</td><td>3</td><td>16.7</td><td>0.216</td></tr><tr><td>Diabetes mellitus</td><td>33</td><td>14.3</td><td>26</td><td>12.2</td><td>7</td><td>38.9</td><td><strong>0.007</strong></td></tr><tr><td>Liver disease</td><td>11</td><td>4.8</td><td>7</td><td>3.3</td><td>4</td><td>22.2</td><td><strong>0.006</strong></td></tr><tr><td>Obesity</td><td>25</td><td>10.8</td><td>24</td><td>11.3</td><td>1</td><td>5.6</td><td>0.701</td></tr><tr><td>Renal impairment</td><td>15</td><td>6.5</td><td>12</td><td>5.6</td><td>3</td><td>16.7</td><td>0.100</td></tr><tr><td>Smoking history</td><td>20</td><td>8.7</td><td>19</td><td>8.9</td><td>1</td><td>5.6</td><td>1.000</td></tr><tr><td><strong>Chronic myeloid leukemia</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>CCI</td><td>3 (2-6) [0-30]</td><td></td><td>3 (2-5) [0-30]</td><td></td><td>6 (6-6) [6-6]</td><td></td><td>0.375</td></tr><tr><td>Month of diagnosis prior to COVID-19 onset</td><td>48 (16-112) [0-372]</td><td></td><td>48 (17-108) [0-372]</td><td></td><td>58 (12-120) [0-245]</td><td></td><td>0.780</td></tr><tr><td>Last malignancy treatment immediately before COVID-19 onset</td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.033</strong></td></tr><tr><td>Drug-based therapies</td><td>215</td><td>93.1</td><td>199</td><td>86.1</td><td>16</td><td>6.9</td><td></td></tr><tr><td><em>In the last month</em></td><td>172</td><td>74.5</td><td>158</td><td>68.4</td><td>14</td><td>6.1</td><td></td></tr><tr><td>1G TKIs (Imatinib)</td><td>77</td><td>33.3</td><td>68</td><td>29.4</td><td>9</td><td>3.9</td><td></td></tr><tr><td><em>Imatinib</em></td><td>77</td><td>33.3</td><td>68</td><td>29.4</td><td>9</td><td>3.9</td><td></td></tr><tr><td>2G TKIs</td><td>76</td><td>32.9</td><td>74</td><td>32.0</td><td>2</td><td>0.9</td><td></td></tr><tr><td><em>Bosutinib</em></td><td>11</td><td>4.8</td><td>11</td><td>4.8</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Dasatinib</em></td><td>36</td><td>15.6</td><td>35</td><td>15.2</td><td>1</td><td>0.4</td><td></td></tr><tr><td><em>Nilotinib</em></td><td>29</td><td>12.6</td><td>28</td><td>12.1</td><td>1</td><td>0.4</td><td></td></tr><tr><td>3G TKIs</td><td>12</td><td>5.2</td><td>11</td><td>4.8</td><td>1</td><td>0.4</td><td></td></tr><tr><td><em>Asciminib</em></td><td>4</td><td>1.7</td><td>4</td><td>1.7</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Ponatinib</em></td><td>8</td><td>3.5</td><td>7</td><td>3.0</td><td>1</td><td>0.4</td><td></td></tr><tr><td>Conventional chemotherapy</td><td>6</td><td>2.6</td><td>5</td><td>2.2</td><td>1</td><td>0.4</td><td></td></tr><tr><td>Demethylating agents</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td>1</td><td>0.4</td><td></td></tr><tr><td><em>In the last 3 months</em></td><td>18</td><td>7.8</td><td>18</td><td>7.8</td><td>0</td><td>0.0</td><td></td></tr><tr><td>1G TKIs</td><td>8</td><td>3.5</td><td>8</td><td>3.5</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Imatinib</em></td><td>8</td><td>3.5</td><td>8</td><td>3.5</td><td>0</td><td>0.0</td><td></td></tr><tr><td>2G TKIs</td><td>6</td><td>2.6</td><td>6</td><td>2.6</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Bosutinib</em></td><td>4</td><td>1.7</td><td>4</td><td>1.7</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Nilotinib</em></td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Conventional chemotherapy</td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Demethylating agents</td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Immunochemotherapy</td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Immunochemotherapy + TKIs</td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>> 3 months</em></td><td>12</td><td>5.2</td><td>11</td><td>4.8</td><td>1</td><td>0.4</td><td></td></tr><tr><td>1G TKIs</td><td>6</td><td>2.6</td><td>6</td><td>2.6</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Imatinib</em></td><td>6</td><td>2.6</td><td>6</td><td>2.6</td><td>0</td><td>0.0</td><td></td></tr><tr><td>2G TKIs</td><td>4</td><td>1.7</td><td>4</td><td>1.7</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Bosutinib</em></td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Dasatinib</em></td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Nilotinib</em></td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td></td></tr><tr><td>3G TKIs</td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Ponatinib</em></td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Demethylating agents</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td>1</td><td>0.4</td><td></td></tr><tr><td><em>Not reported</em></td><td>13</td><td>5.6</td><td>12</td><td>5.2</td><td>1</td><td>0.4</td><td></td></tr><tr><td>1G TKIs</td><td>5</td><td>2.2</td><td>5</td><td>2.2</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Imatinib</em></td><td>5</td><td>2.2</td><td>5</td><td>2.2</td><td>0</td><td>0.0</td><td></td></tr><tr><td>2G TKIs</td><td>7</td><td>3.0</td><td>6</td><td>2.6</td><td>1</td><td>0.4</td><td></td></tr><tr><td><em>Dasatinib</em></td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>Nilotinib</em></td><td>5</td><td>2.2</td><td>4</td><td>1.7</td><td>1</td><td>0.4</td><td></td></tr><tr><td>Conventional chemotherapy</td><td>1</td><td>0.4</td><td>1</td><td>0.4</td><td>0</td><td>0.0</td><td></td></tr><tr><td>HSCT therapies</td><td>10</td><td>4.3</td><td>9</td><td>3.9</td><td>1</td><td>0.4</td><td></td></tr><tr><td><em>In the last 6 months</em></td><td>4</td><td>1.7</td><td>4</td><td>1.7</td><td>0</td><td>0.0</td><td></td></tr><tr><td><em>> 6 months</em></td><td>6</td><td>2.6</td><td>5</td><td>2.2</td><td>1</td><td>0.4</td><td></td></tr><tr><td>No treatment</td><td>6</td><td>2.6</td><td>5</td><td>2.2</td><td>1</td><td>0.4</td><td></td></tr><tr><td><strong>Status malignancy at COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.009</strong></td></tr><tr><td>Controlled disease</td><td>173</td><td>74.9</td><td>165</td><td>77.5</td><td>8</td><td>44.4</td><td></td></tr><tr><td>Stable disease</td><td>27</td><td>11.7</td><td>23</td><td>10.8</td><td>4</td><td>22.2</td><td></td></tr><tr><td>Active disease</td><td>27</td><td>11.7</td><td>22</td><td>10.3</td><td>5</td><td>27.8</td><td></td></tr><tr><td>Unknown</td><td>4</td><td>1.7</td><td>3</td><td>1.4</td><td>1</td><td>5.6</td><td></td></tr><tr><td><strong>Vaccination status at COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.081</strong></td></tr><tr><td>Not vaccinated</td><td>175</td><td>75.8%</td><td>158</td><td>74.2%</td><td>17</td><td>94.4%</td><td></td></tr><tr><td>Vaccinated</td><td>56</td><td>24.2%</td><td>55</td><td>25.8%</td><td>1</td><td>5.6%</td><td></td></tr></tbody></table>

CCI: Charlson comorbidity index; G TKIs: generation tyrosine kinase inhibitor; HSCT: hematopoietic stem cell transplantation
<figure><img src="image_17.png" /></figure>

role of TKIs [22]. *In vitro* experiments have indicated that imatinib may block the fusion of the coronavirus's Spike protein with cell membranes, thereby preventing virus activation and endocytosis [23–25].

In this analysis, approximately one-fourth of the CML patients received vaccination, and among them, the

mortality rate was 1.7% (1 out of 56 patients). In contrast, the mortality rate for unvaccinated patients was 9.7%. In 2022, out of 46 patients, 76.1% were vaccinated, and no critical infections, ICU admissions, or deaths were recorded among these vaccinated patients. A study evaluating the outcomes of serological testing

<table><caption>Table 2. Clinical features of COVID-19 in CML patients.</caption><thead><tr><th rowspan="2"></th><th colspan="2">Overall</th><th colspan="2">Alive</th><th colspan="2">Dead</th><th rowspan="2">p value</th></tr><tr><th>n</th><th>%</th><th>n</th><th>%</th><th>n</th><th>%</th></tr></thead><tbody><tr><td><strong>Symptoms at COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.001</strong></td></tr><tr><td>Pulmonary</td><td>116</td><td>50.2</td><td>109</td><td>51.2</td><td>7</td><td>38.9</td><td></td></tr><tr><td>Pulmonary + extrapulmonary</td><td>54</td><td>23.4</td><td>48</td><td>22.5</td><td>6</td><td>33.3</td><td></td></tr><tr><td>Extrapulmonary</td><td>57</td><td>24.7</td><td>55</td><td>25.8</td><td>2</td><td>11.1</td><td></td></tr><tr><td>Screening</td><td>4</td><td>1.7</td><td>1</td><td>0.5</td><td>3</td><td>16.7</td><td></td></tr><tr><td><strong>COVID-19 status</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>&lt;0.001</strong></td></tr><tr><td>Asymptomatic</td><td>50</td><td>21.6</td><td>50</td><td>23.5</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Mild infection</td><td>99</td><td>42.9</td><td>95</td><td>44.6</td><td>4</td><td>22.2</td><td></td></tr><tr><td>Severe infection</td><td>66</td><td>28.6</td><td>61</td><td>28.6</td><td>5</td><td>27.8</td><td></td></tr><tr><td>Critical infection</td><td>16</td><td>6.9</td><td>7</td><td>3.3</td><td>9</td><td>50.0</td><td></td></tr><tr><td><strong>Neutrophils at COVID-19 onset (x109/mm3)</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>1.000</strong></td></tr><tr><td>&lt;0.501</td><td>1</td><td>0.4</td><td>1</td><td>0.5</td><td>0</td><td>0.0</td><td></td></tr><tr><td>0.501-0.999</td><td>5</td><td>2.2</td><td>5</td><td>2.3</td><td>0</td><td>0.0</td><td></td></tr><tr><td>&gt;0.999</td><td>161</td><td>69.7</td><td>145</td><td>68.1</td><td>16</td><td>88.9</td><td></td></tr><tr><td><strong>Lymphocytes at COVID-19 onset (x109/mm3)</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.030</strong></td></tr><tr><td>&lt;0.201</td><td>4</td><td>1.7</td><td>3</td><td>1.4</td><td>1</td><td>5.6</td><td></td></tr><tr><td>0.201-0.499</td><td>9</td><td>3.9</td><td>6</td><td>2.8</td><td>3</td><td>16.7</td><td></td></tr><tr><td>&gt;0.499</td><td>157</td><td>68.0</td><td>144</td><td>67.6</td><td>13</td><td>72.2</td><td></td></tr><tr><td><strong>Stay during COVID-19</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Home</td><td>149</td><td>64.5</td><td>148</td><td>69.5</td><td>1</td><td>5.6</td><td><strong>&lt;0.001</strong></td></tr><tr><td>Hospital</td><td>96</td><td>41.6</td><td>78</td><td>36.6</td><td>18</td><td>100.0</td><td><strong>&lt;0.001</strong></td></tr><tr><td>Duration in days</td><td>13 (6.5-21.5)</td><td>[1-130]</td><td>11 (6-21)</td><td>[1v130]</td><td>14 (11-30)</td><td>[2-50]</td><td>0.125</td></tr><tr><td>ICU</td><td>16</td><td>6.9</td><td>7</td><td>3.3</td><td>9</td><td>50.0</td><td><strong>&lt;0.001</strong></td></tr><tr><td>Non-invasive ventilation</td><td>5</td><td>2.2</td><td>2</td><td>0.9</td><td>3</td><td>16.7</td><td>1.000</td></tr><tr><td>Invasive ventilation</td><td>8</td><td>3.5</td><td>4</td><td>1.9</td><td>4</td><td>22.2</td><td></td></tr><tr><td>Duration in days</td><td>12 (6-20)</td><td>[1-115]</td><td>27 (13-40)</td><td>[1-115]</td><td>8 (5-12)</td><td>[2-20]</td><td>0.073</td></tr><tr><td><strong>COVID-19 treatment</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.385</strong></td></tr><tr><td>No specific treatment reported</td><td>92</td><td>39.8</td><td>87</td><td>40.8</td><td>5</td><td>27.8</td><td></td></tr><tr><td>Antivirals ± corticosteroids ± plasma</td><td>12</td><td>5.2</td><td>12</td><td>5.6</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Antivirals + monoclonal<br/>antibodies ± corticosteroids ± plasma</td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Monoclonal<br/>antibodies ± corticosteroids ± plasma</td><td>8</td><td>3.5</td><td>8</td><td>3.8</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Plasma ± corticosteroids</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td></td></tr><tr><td>Corticosteroids</td><td>10</td><td>4.3</td><td>8</td><td>3.8</td><td>2</td><td>11.1</td><td></td></tr><tr><td>Unknown</td><td>107</td><td>46.3</td><td>96</td><td>45.1</td><td>11</td><td>61.1</td><td></td></tr><tr><td><strong>Hematologic grade 3-4 TKIs-related adverse events during COVID-19</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Anemia</td><td>7</td><td>3.0</td><td>6</td><td>2.8</td><td>1</td><td>5.6</td><td>0.258</td></tr><tr><td>Bleeding</td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Neutropenia</td><td>5</td><td>2.2</td><td>4</td><td>1.9</td><td>1</td><td>5.6</td><td>0.189</td></tr><tr><td>Thrombocytopenia</td><td>4</td><td>1.7</td><td>3</td><td>1.4</td><td>1</td><td>5.6</td><td>0.154</td></tr><tr><td>Thrombosis</td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>None of the above</td><td>63</td><td>27.3</td><td>62</td><td>29.1</td><td>1</td><td>5.6</td><td>0.065</td></tr><tr><td>Unknown</td><td>148</td><td>64.1</td><td>134</td><td>62.9</td><td>14</td><td>77.8</td><td></td></tr><tr><td><strong>Non-hematologic TKIs-related adverse events during COVID-19</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Cardiac</td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Gastrointestinal</td><td>3</td><td>1.3</td><td>3</td><td>1.4</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Hepatotoxicity</td><td>1</td><td>0.4</td><td>1</td><td>0.5</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Infections (bacterial, fungal)</td><td>1</td><td>0.4</td><td>1</td><td>0.5</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Musculoskeletal</td><td>4</td><td>1.7</td><td>4</td><td>1.9</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Neurological</td><td>1</td><td>0.4</td><td>1</td><td>0.5</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Pulmonary</td><td>5</td><td>2.2</td><td>4</td><td>1.9</td><td>1</td><td>5.6</td><td>0.189</td></tr><tr><td>Renal impairment</td><td>2</td><td>0.9</td><td>2</td><td>0.9</td><td>0</td><td>0.0</td><td>1.000</td></tr><tr><td>Others</td><td>2</td><td>0.9</td><td>1</td><td>0.5</td><td>1</td><td>5.6</td><td>0.079</td></tr><tr><td>None of the above</td><td>62</td><td>26.8</td><td>61</td><td>28.6</td><td>1</td><td>5.6</td><td>0.076</td></tr><tr><td>Unknown</td><td>148</td><td>64.1%</td><td>133</td><td>62.4%</td><td>15</td><td>83.3%</td><td></td></tr><tr><td><strong>Mortality</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td><strong>0.001</strong></td></tr><tr><td>Observation days</td><td>68.5 (22-235)</td><td>[0-815]</td><td>78 (24-252)</td><td>[0-815]</td><td>15 (11-61)</td><td>[0-509]</td><td></td></tr><tr><td><strong>Reason for mortality</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>COVID-19</td><td>14</td><td>6.1</td><td>0</td><td>0.0</td><td>14</td><td>77.8</td><td></td></tr><tr><td>COVID-19 + haematological malignancy</td><td>4</td><td>1.7</td><td>0</td><td>0.0</td><td>4</td><td>22.2</td><td></td></tr></tbody></table>
<figure><img src="image_18.png" /><figcaption>**Table 3.** Overall mortality predictors in COVID-19 CML patients.</figcaption></figure>

<table><thead><tr><th rowspan="3"></th><th colspan="4">Univariable analysis</th><th colspan="4">Multivariable analysis</th></tr><tr><th rowspan="2">p value</th><th rowspan="2">HR</th><th colspan="2">95% CI</th><th rowspan="2">p value</th><th rowspan="2">HR</th><th colspan="2">95% CI</th></tr><tr><th>Lower limit</th><th>Lower limit</th><th>Lower limit</th><th>Upper limit</th></tr></thead><tbody><tr><td><strong>Sex</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Female</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Male</td><td>0.976</td><td>0.986</td><td>0.389</td><td>2.500</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Age</strong></td><td><strong>0.009</strong></td><td><strong>1.043</strong></td><td><strong>1.010</strong></td><td><strong>1.076</strong></td><td><strong>0.011</strong></td><td><strong>1.043</strong></td><td><strong>1.010</strong></td><td><strong>1.078</strong></td></tr><tr><td><strong>Status malignancy at COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Controlled disease</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Stable disease</td><td>0.066</td><td>3.092</td><td>0.929</td><td>10.286</td><td><strong>0.021</strong></td><td>4.680</td><td>1.256</td><td>17.438</td></tr><tr><td>Active disease</td><td><strong>0.011</strong></td><td>4.266</td><td>1.395</td><td>13.048</td><td>0.056</td><td>3.096</td><td>0.971</td><td>9.875</td></tr><tr><td>Unknown</td><td><strong>0.035</strong></td><td>9.615</td><td>1.176</td><td>78.581</td><td>0.266</td><td>3.483</td><td>0.386</td><td>31.412</td></tr><tr><td>Comorbidities at COVID-19 onset</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>No comorbidities</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>1 comorbidity</td><td>0.066</td><td>3.666</td><td>0.916</td><td>14.670</td><td></td><td></td><td></td><td></td></tr><tr><td>2 comorbidities</td><td><strong>0.015</strong></td><td>5.887</td><td>1.404</td><td>24.676</td><td></td><td></td><td></td><td></td></tr><tr><td>3 or more comorbidities</td><td><strong>0.009</strong></td><td>7.412</td><td>1.657</td><td>33.156</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>COVID-19 status</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Asymptomatic</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Mild infection</td><td>0.926</td><td>-</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Severe infection</td><td>0.922</td><td>-</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Critical infection</td><td>0.906</td><td>-</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Chronic cardiopathy</strong></td><td><strong>0.007</strong></td><td>3.629</td><td>1.430</td><td>9.209</td><td>0.804</td><td>0.848</td><td>0.232</td><td>3.103</td></tr><tr><td><strong>Chronic pulmonary disease</strong></td><td>0.271</td><td>2.008</td><td>0.581</td><td>6.939</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Diabetes mellitus</strong></td><td><strong>0.005</strong></td><td>3.859</td><td>1.492</td><td>9.981</td><td>0.495</td><td>1.511</td><td>0.461</td><td>4.952</td></tr><tr><td><strong>Liver disease</strong></td><td><strong>0.002</strong></td><td>5.715</td><td>1.872</td><td>17.446</td><td>0.058</td><td>3.021</td><td>0.962</td><td>9.489</td></tr><tr><td><strong>Obesity</strong></td><td>0.348</td><td>0.380</td><td>0.050</td><td>2.871</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Renal impairment</strong></td><td>0.080</td><td>3.048</td><td>0.877</td><td>10.599</td><td>0.374</td><td>2.024</td><td>0.428</td><td>9.571</td></tr><tr><td>Smoking history</td><td>0.718</td><td>0.689</td><td>0.092</td><td>5.187</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Last malignancy treatment immediately before COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>No treatment</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>1G TKIs (Imatinib)</td><td>0.622</td><td>0.593</td><td>0.074</td><td>4.740</td><td></td><td></td><td></td><td></td></tr><tr><td>2G TKIs (Bosutinib, Dasatinib, Nilotinib)</td><td>0.131</td><td>0.174</td><td>0.018</td><td>1.688</td><td></td><td></td><td></td><td></td></tr><tr><td>3G TKIs (Asciminib, Ponatinib)</td><td>0.580</td><td>0.457</td><td>0.029</td><td>7.324</td><td></td><td></td><td></td><td></td></tr><tr><td>alloHSCT</td><td>0.978</td><td>0.962</td><td>0.060</td><td>15.492</td><td></td><td></td><td></td><td></td></tr><tr><td>Conventional chemotherapy</td><td>0.972</td><td>0.952</td><td>0.059</td><td>15.268</td><td></td><td></td><td></td><td></td></tr><tr><td>Demethylating agents</td><td>0.084</td><td>8.720</td><td>0.750</td><td>101.318</td><td></td><td></td><td></td><td></td></tr><tr><td>Immunochemotherapy</td><td>0.985</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Immunochemotherapy + TKIs</td><td>0.996</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Anti-SARS-CoV-2 vaccination</strong></td><td>0.237</td><td>0.293</td><td>0.038</td><td>2.243</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>SARS-CoV-2 variant</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Wild type</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Delta</td><td>0.996</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Omicron</td><td>0.983</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Not tested</td><td>0.415</td><td>0.432</td><td>0.057</td><td>3.258</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Neutrophils at COVID-19 onset (×109/mm3)</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>&lt;0.501</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>0.501–0.999</td><td>0.914</td><td>0.883</td><td>0.091</td><td>8.585</td><td></td><td></td><td></td><td></td></tr><tr><td>&gt;0.999</td><td>0.193</td><td>0.259</td><td>0.034</td><td>1.984</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Lymphocytes at COVID-19 onset (×109/mm3)</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>&lt;0.201</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>0.201–0.499</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>&gt;0.499</td><td>0.632</td><td>21.218</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Symptoms at COVID-19 onset</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Pulmonary</td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td></tr><tr><td>Pulmonary + extrapulmonary</td><td>0.141</td><td>2.278</td><td>0.761</td><td>6.821</td><td>0.547</td><td>0.638</td><td>0.148</td><td>2.747</td></tr><tr><td>Extrapulmonary</td><td>0.533</td><td>0.607</td><td>0.126</td><td>2.923</td><td>0.957</td><td>0.953</td><td>0.169</td><td>5.385</td></tr><tr><td>Screening</td><td><strong>&lt;0.001</strong></td><td>17.611</td><td>4.449</td><td>69.720</td><td>0.863</td><td>0.810</td><td>0.074</td><td>8.894</td></tr><tr><td><strong>ICU admission</strong></td><td><strong>&lt;0.001</strong></td><td>15.125</td><td>5.934</td><td>38.553</td><td><strong>&lt;0.001</strong></td><td>13.349</td><td>4.594</td><td>38.789</td></tr><tr><td><strong>COVID-19 treatment</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>No specific treatment reported</td><td>-</td><td>-</td><td>-</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Antivirals ± corticosteroids ± plasma</td><td>0.989</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Antivirals + monoclonal antibodies ± corticosteroids ± plasma</td><td>0.996</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Monoclonal antibodies ± corticosteroids ± plasma</td><td>0.990</td><td>0.000</td><td>0.000</td><td>-</td><td></td><td></td><td></td><td></td></tr><tr><td>Corticosteroids</td><td>0.143</td><td>3.443</td><td>0.659</td><td>17.992</td><td></td><td></td><td></td><td></td></tr><tr><td>Unknown</td><td>0.253</td><td>1.864</td><td>0.641</td><td>5.419</td><td></td><td></td><td></td><td></td></tr></tbody></table>

HR: hazard ratio; G TKIs: generation tyrosine kinase inhibitor
<figure><img src="image_19.png" /></figure>

<figure><img src="image_20.png" /><figcaption>**Figure 2.** Overall survival across years.</figcaption></figure>

in CML patients revealed similarities to the general population, indicating that CML patients can generate an adequate antibody response to SARS-CoV-2 [26–28]. Despite the risk of impaired antibody production in many patients with hematological malignancies, the rate of seronegative patients after COVID-19 vaccination was reported to be 2.9% in CML patients [29]. Furthermore, CML patients using TKIs exhibited a higher response to mRNA COVID-19 vaccination compared to other hematologic malignancies, and the response was nearly comparable to that observed in healthy individuals [30]. Additionally, after receiving the vector-based vaccine GamCOVIDVac (Sputnik V), chronic phase CML patients demonstrated a seroconversion rate of about 93–94% [31]. The robust response to COVID-19 vaccination may have a positive impact on the survival of CML patients following COVID-19 infection. In a matched cohort study involving chronic phase CML patients, those who did not receive a COVID-19 vaccination were found to have an increased risk of hospitalization compared to the control group [32].

In our study, approximately 40% of the patients were hospitalized, with a median hospital stay of 13 d. The overall mortality rate was 7.8%, and this rate decreased over the course of the pandemic. Among the patients identified in 2020 without a COVID-19 vaccine, 142 (61.5%) had a higher risk of experiencing severe and life-threatening infections, requiring hospitalization, ICU admission, and facing mortality compared to patients identified in 2021 and 2022. The results of the

multivariable analysis revealed that age, stable malignancy status, and ICU admission were significant independent factors associated with mortality. These findings further confirm the beneficial effect of vaccination in CML patients. Moreover, the results illustrate that, within our patient sample, individuals with active malignancies faced a reduced risk of mortality in comparison to the patients with a stable malignancy. This observation might be attributed to the predominance of newly onset malignancies rather than refractory cases.

This study has several limitations, including its retrospective design and a small number of patients. Additionally, the survey did not clearly define the status of CML patients, as it relied on practitioners' indications of whether the disease was active, controlled, or stable. The Sokal or Hasford scores, which are commonly used to assess the severity and prognosis of CML, were not monitored in the database. It is important to note that our survey may not capture the entirety of CML cases from each participating institution, and there is no means to ascertain whether all institutions contributed all their CML cases. Additionally, given the longitudinal nature of our sample, it's noteworthy that the overall vaccination rate could be perceived as relatively low. Various factors may contribute to this, including vaccine availability in the respective country, medical advice provided by physicians, and individual patient decisions.

In conclusion, this large database supports the finding that the majority of CML patients experience mild cases of COVID-19 during the pandemic. The incidence
<figure><img src="image_21.png" /></figure>

of mortality is low and has decreased over time. Furthermore, vaccinations have shown to be highly effective in CML patients. The beneficial effects of COVID-19 vaccinations in CML patients are reflected in the lower mortality rates and reduced occurrence of severe COVID-19 infections.

## Collaborators (to be mentioned in PubMed)

Sofia ZOMPI, Ayel Omar YAHIA, Toni VALKOVIĆ, Panagiotis TSIRIGOTIS, Zlate STOJANOSKI, Andrés SOTO-SILVA, Uluhan SILI, Alexandra SERRIS, Juergen PRATTES, Klára PIUKOVICS, Joseph MELETIADIS, Marina MACHADO, Marie-Pierre LEDOUX, Tobias LAHMER, Moraima JIMÉNEZ, Ozren JAKSIC, José-Ángel HERNÁNDEZ-RIVAS, Carolina GARCIA-VIDAL, Guillemette FOUQUET, Noemí FERNÁNDEZ, Rita FAZZI, Iker FALCES-ROMERO, Noha EISA, Michelina DARGENIQ, Milche CVETANOSKI, Annarosa CUCCARO, Gökçe Melis ÇOLAK, Martin ČERŇAN, Alba CABIRTA, Alessandro BUSCA, Anastasia ANTONIADOU, Tommaso Francesco AEILLO, Ghaith ABU-ZEINAH

## Disclosure statement

No potential conflict of interest was reported by the author(s).

## Funding

This work was supported by Optics COMMIT (COVID-19 Unmet Medical Needs and Associated Research Extension) COVID-19 RFP program by GILEAD Science, United States [2020-8223].

## ORCID

Shaimaa El-Ashwah ID http://orcid.org/0000-0003-2210-1534
Jon Salmanton-García ID http://orcid.org/0000-0002-6766-8297
Yavuz M. Bilgin ID http://orcid.org/0000-0002-3783-3407
Federico Itri ID http://orcid.org/0000-0002-3532-5281
Pavel Žák ID http://orcid.org/0000-0003-4465-5343
Barbora Weinbergerová ID http://orcid.org/0000-0001-6460-2471
Luisa Verga ID http://orcid.org/0000-0002-0868-3358
Ali S. Omrani ID http://orcid.org/0000-0001-5309-6358
Maria Gomes da Silva ID http://orcid.org/0000-0002-6993-2450
Monia Marchetti ID http://orcid.org/0000-0001-7615-0572
Caterina Buquicchio ID http://orcid.org/0000-0002-3683-5953
Marcio Nucci ID http://orcid.org/0000-0003-4867-0014
Martin Schönlein ID http://orcid.org/0000-0002-1010-0975
Francesca Farina ID http://orcid.org/0000-0002-5124-6970
Caroline Besson ID http://orcid.org/0000-0003-4364-7173
Lucia Prezioso ID http://orcid.org/0000-0003-1660-4960

Julio Dávila-Valls ID http://orcid.org/0000-0002-5185-2073
Sonia Martín-Pérez ID http://orcid.org/0000-0001-5809-7165
Valentina Bonuomo ID http://orcid.org/0000-0001-6491-8337
Jaap Van Doesum ID http://orcid.org/0000-0003-0214-3219
Maria Chiara Tisi ID http://orcid.org/0000-0001-8231-6700
Francesco Passamonti ID http://orcid.org/0000-0001-8068-5289
Gustavo-Adolfo Méndez ID http://orcid.org/0000-0003-0514-7004
Stef Meers ID http://orcid.org/0000-0003-1754-2175
Johan Maertens ID http://orcid.org/0000-0003-4257-5980
Alberto López-García ID http://orcid.org/0000-0002-5354-5261
Andreas Glenthøj ID http://orcid.org/0000-0003-2082-0738
Matteo Bonnani ID http://orcid.org/0000-0003-1775-6333
Irati Ormazabal-Vélez ID http://orcid.org/0000-0003-1141-5546
Jorge Labrador ID http://orcid.org/0000-0002-3696-0287
Austin Kulasekararaj ID http://orcid.org/0000-0003-3180-3570
Ildefonso Espigado ID http://orcid.org/0000-0002-4043-6613
Fatih Demirkan ID http://orcid.org/0000-0002-1172-8668
Nick De Jonge ID http://orcid.org/0000-0002-9901-0887
Maria Calbacho ID http://orcid.org/0000-0001-8106-4863
Ola Blennow ID http://orcid.org/0000-0002-7167-7882
Murtadha Al-Khabori ID http://orcid.org/0000-0002-2937-8838
Miloš Mladenović ID http://orcid.org/0000-0002-8350-2182
Zdeněk Ráčil ID http://orcid.org/0000-0003-3511-4596
Emanuele Ammatuna ID http://orcid.org/0000-0001-8247-4901
Raul Cordoba ID http://orcid.org/0000-0002-7654-8836
Ditte Stampe Hersby ID http://orcid.org/0000-0002-2999-8949
Stefanie Gräfe ID http://orcid.org/0000-0001-7678-0179
Ziad Emarah ID http://orcid.org/0000-0003-0622-2598
Maria Vittoria Sacchi ID http://orcid.org/0000-0001-8133-3357
Laman Rahimli ID http://orcid.org/0000-0003-2266-445X
Raquel Nunes Rodrigues ID http://orcid.org/0000-0002-8347-4281
Giovanni Paolo Maria Zambrotta ID http://orcid.org/0000-0002-8612-2994
Francesco Marchesi ID http://orcid.org/0000-0001-6353-2272
Oliver A. Cornely ID http://orcid.org/0000-0001-9599-3137
Livio Pagano ID http://orcid.org/0000-0001-8287-928X

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