key: cord-0994203-tsqpnlo8
authors: Belsky, Jennifer A.; Tullius, Brian P.; Lamb, Margaret G.; Sayegh, Rouba; Stanek, Joseph R.; Auletta, Jeffery J.
title: COVID-19 in immunocompromised patients: a systematic review of cancer, hematopoietic cell and solid organ transplant patients
date: 2021-02-04
journal: J Infect
DOI: 10.1016/j.jinf.2021.01.022
sha: 16258272a240b54fb06f6002a2c677411cd3c981
doc_id: 994203
cord_uid: tsqpnlo8

BACKGROUND: The clinical impact of severe coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), in immunocompromised patients has not been systematically evaluated. METHODS: We reviewed current literature reporting on COVID-19 in cancer (CA), hematopoietic cell (HCT), and solid organ transplant (SOT) patients and compared their clinical data and outcomes to the general population. For adult CA, HCT and SOT patients, an extensive search strategy retrieved all articles published until July 20, 2020 by combining the terms coronavirus, coronavirus infection, COVID-19, and SARS-CoV-2 in PubMed, Cochrane, and Web of Science, and following the Preferred Reporting Items for Systematic Reviews and Meta-analysis guidelines. For the pediatric CA cohort, a global COVID-19 registry was used. For the general population cohort, a large meta-analysis was used to compare pooled prevalence estimates, and two large meta-analyses were utilized to serve as pooled comparators for hospitalized COVID-19 patients. FINDINGS: Compared to the general population, adult CA and SOT patients with COVID-19 had higher comorbidities, greater levels of inflammatory markers at diagnosis, and higher rates of intensive care and hospital mortality. Pediatric CA patients and HCT patients with COVID-19 tended to have clinical presentations and outcomes similar to the general population. INTERPRETATION: To our knowledge, this is the first systematic review evaluating COVID-19 phenotype and outcomes in immunocompromised patients and comparing them to the general population, which shows that hospital outcomes appear to be worse in adult CA and SOT patients, potentially due to their higher co-morbidity burden. FUNDING: None

The Coronavirus Disease 2019 (COVID-19) pandemic caused by the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has afflicted millions of people around the world, resulting in nearly one million deaths. 1 COVID-19 is primarily characterized by fever and lower respiratory symptoms but can range in severity from asymptomatic to critical illness with acute respiratory distress syndrome (ARDS), septic shock, multiorgan failure and death. While the strongest predictor of hospitalization and death is age >65 years, patients with comorbidities at any age are at higher risk of severe disease. [2] [3] [4] [5] As our understanding of COVID-19 evolves, it is becoming apparent that there are two phases of the diseasean initial immunosuppressive state allowing viral replication followed by a hyperinflammatory response leading to worsening respiratory failure and shock. 6, 7 Viral escape from immune surveillance is demonstrated by both quantitative [8] [9] [10] [11] and qualitative 12, 13 suppression of NK cells and depletion of CD8 + T cells [14] [15] [16] in patients with severe disease. Therefore, stunting the immune response early in the infection could potentially enable uncontrolled viral replication and clinical progression to severe disease. Given this pathophysiology, immunocompromised patients may be at higher risk for severe COVID-19.

Cancer (CA), hematopoietic cell transplant (HCT), and solid organ transplant (SOT) patients compromise a significant proportion of immunocompromised patients, a heterogeneous population with primary (inheritable) and secondary (acquired) immune abnormalities. 17 In 2018, an estimated 1,735,350 people were newly diagnosed with CA in the United States. 18 In the same year, 36,529 SOTs 19 and 14,006 autologous and 9,028 allogeneic HCTs 20 were performed in the United States. Immune-based pharmaceutical and cellular therapies have transformed outcomes in these patients by reducing malignant disease relapse, 21 preventing or attenuating deleterious alloreactivity (i.e., graft rejection or graft-versus-host disease) and inflammation, 22 or augmenting antimicrobial immunity. 23 Some of these same immunomodulatory therapies have also been used to treat severe COVID-19. 24, 25 Despite an emerging literature on COVID-19 in immunocompromised patients, a comprehensive review defining the clinical impact of COVID-19 in CA, HCT and SOT patients and comparing outcomes with the general population has not been performed. Therefore, we performed a systematic review of COVID-19 defining clinical features, laboratory testing, therapeutic interventions and outcomes in immunocompromised patients and then compared these results to the general population with COVID-19.

We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses screened articles. When research produced more than one published study utilizing the same data, only articles that presented disparate enough data were included. Otherwise, only the more comprehensive and recent study was included.

Publications meeting the initial search criteria were evaluated for inclusion in the current study.

To be included, the study must have reported clinical data on adult (A-CA) or pediatric (P-CA) cancer patients and SOT or HCT recipients with confirmed COVID-19. Our inclusion and exclusion criteria identified 64 SOT studies, 11 HCT studies, 91-101 25 A-CA studies, and one global P-CA database, 127 the COVID-19 and Childhood Cancer Registry (CCCR) Table 1 ). The CCCR is a global COVID-19 observatory resource center through the Global COVID-19 Observatory and Resource Center for Childhood Cancer, a collaborative effort between St. Jude Children's Research Hospital (SJCRH) and the International Society of Paediatric Oncology (SIOP). The database was initially accessed in June 2020 and data was extracted through July 20, 2020, which included patient demographics and COVID-19 risk factors, illness severity, clinical/laboratory data, outcomes, and treatment. The CCCR was used for P-CA data given its volume of reported patients and the incomplete data reported in case reports and small case series, which compromise the majority of the published COVID-19 experience in the P-CA population, resulting in the inability to ensure that data from these publications were not duplicated in the registry.

In order to compare characteristics of COVID-19 with the immunocompromised cohorts, a large meta-analysis of COVID-19 patients (n=61,742) 128 was selected as the general population cohort, given the publication presented patient data in a manner comparable to our study with similar pooled prevalence analyses as described below. Within this cohort, 2·7% (95% CI 0·4-7·4) of patients had CA and where thus immunocompromised, which is within the incidence rate for CA within the general population (8·3%, standard error 0·17). 129 Therefore, the CA patient data was not separated from the general population data. For a comparator from hospitalized COVID-19 patients from the general population, we combined data from 2 large metaanalyses 130, 131 (total n=11,721) with patient data similar to our meta-analysis.

Following initial screen, three independent reviewers (J.A.B., R.S., M.G.L.) extracted available data. Discrepancies were resolved by discussion and consensus with a fourth independent reviewer (J.J.A). Each study was evaluated for patient demographic data including patient age at time of COVID-19 diagnosis, comorbidities, time from transplant to COVID-19 diagnosis (SOT and HCT), organ transplanted (SOT), transplant indication (HCT), transplant-related immunosuppression in the (SOT), and type of malignancy (A-CA and P-CA). Similarly, each study was evaluated for prevalence of COVID-19 symptoms (fever, fatigue, myalgia, cough, dyspnea, abdominal pain, vomiting, diarrhea, anosmia/dysgeusia, and neurologic symptoms such as headache). However, data from a given study was only utilized if the study explicitly referenced the presence or absence of a given symptom.

Laboratory data including hematologic indices and inflammatory markers [procalcitonin (PCT), C-reactive protein (CRP), erythrocyte sedimentation rate (ESR), D-dimer, ferritin, lactose dehydrogenase (LDH), and interleukin 6 (IL-6)] during a patient's course of COVID-19 were also extracted. Leukopenia and lymphopenia were defined as white blood cell count (WBC) less than 4,500/L and absolute lymphocyte count (ALC) less than 1,000/L, respectively.

Each study was evaluated for highest COVID-19 severity experienced by reported patients during their illness. Where studies did not explicitly state the severity of their cohort, attempts were made to classify patients based upon their reported clinical data according to the Infectious Disease Society of America criteria as either mild/moderate or severe (pneumonia, ARDS or intensive care management). If not possible, studies were excluded from analyses of COVID-19 severity. Data on hospitalization rates, need for intensive care unit (ICU), and mortality were also recorded. Where not explicitly stated as being in the ICU, patients were included as receiving "intensive care" if they needed invasive or non-invasive ventilatory support or inotropic therapy. Type and frequency of use for all attempted COVID-19 therapeutics were extracted, including modification of baseline immunosuppression (SOT) or of antineoplastic therapies (A-CA and P-CA). The HCT literature did not report alteration in immunosuppression.

Pooled proportional estimates and their 95% confidence intervals (CI) for symptoms, comorbidities, and outcomes were calculated using a random effect model with Freeman-Tukey double arcsine transformation. 132, 133 Heterogeneity of included studies were assessed by calculating I 2 statistics. Nearly every pooled analysis showed some degree of heterogeneity among the included studies with the degree of heterogeneity varying widely (Supplemental Table   2 ). Continuous variables, such as lab values, were presented as medians and interquartile ranges (IQR) either as listed explicitly in the studies or calculated from individual patient values. These variables were summarized descriptively. Demographic data and disease characteristics were summarized descriptively. Statistical analyses were performed using the base R package (R Foundation for Statistical Computing, Vienna, Austria) with the "meta" package and GraphPad Prism 8 (GraphPad Software, San Diego, California).

There was no funding source for this study.

The SOT cohort included kidney (n=675, 59·7%), liver (n=295, 26·1%), heart (n=77, 6·8%), multiple/other (n=34, 3·0%) and lung (n=50, 4·4%). Median patient age ranged from 0·5 to 73·6 years with 50% studies having median age >57 years. Median time from SOT to COVID-19 diagnosis ranged from 0 to 26 years with 50% of studies reporting a median time from transplant >four years.

Within the HCT cohort, 74·2% (n=23) were allogeneic and 22·6% (n=seven) were autologous transplants with one chimeric antigen receptor T cell recipient reported. Median patient age ranged from 10·5 to 64 years with 50% of studies reporting median age ≥59 years. Median time from HCT to COVID-19 diagnosis ranged from 77 days to three years with 50% of studies reporting median time to infection ≥255 days.

The cancer (CA) cohort included adult (A) and pediatrics (P) patients. A-CA patients primarily had solid tumors (n=2,360, 74·8%) and hematologic malignancies (n=653, 20·7%). Median patient age ranged from 32 to 76 years with 50% of studies reporting a median age ≥63 years. P-CA patients had acute lymphoblastic leukemia (n=316, 50·7%), other hematologic malignancy (n=101, 16·2%), extracranial solid tumor (n=159, 25·6%), and central nervous system malignancy (n=47, 7·5%). Nearly 60% of pediatric patients were less than ten years with the remainder between the ages of ten and 18. Patient characteristics are displayed in Supplemental 

Consistent with the general population, 128 hypertension was the most common comorbidity in adult immunocompromised patients with COVID-19 ( Figure 2A ). In general, immunocompromised adults had more baseline comorbidities than general population COVID-19 patients as represented by the gray rectangles. Specifically, the SOT and A-CA had more comorbid cardiovascular disease [20·76% (95% CI 14·63-27·49) and 16·71% (95% CI 9·54-25·12), respectively] and hypertension [74·97% (95% CI 66·75-82·49) and 39·86% (95% CI 31·56-48·43), respectively] than the general population. In addition, SOT patients had a higher incidence of diabetes 39·19% (95% CI, 32·86-45·69). P-CA patients had lesser amounts of comorbidities among the immunocompromised. However, the pediatric population was as comorbid in the areas of cardiovascular and pulmonary disease as adults with COVID-19 from the general population.

In general, the most frequent symptoms reported in immunocompromised patients were fever and cough, consistent with what is reported in the general population with COVID-19 ( Figure   2B ). SOT patients experienced markedly more dyspnea [46·63% (95% CI 38·83-54·5)] than the general population. P-CA patients had lower pooled prevalence of fever, fatigue, myalgia, cough, dyspnea and neurologic symptoms versus both other immunocompromised cohorts and the general population. Anosmia and dysgeusia were inconsistently and rarely reported. With the exception of the P-CA cohort in whom 29·46% patients are reported in the CCCR to have asymptomatic infection, 127 the rate of asymptomatic disease in the other immunocompromised cohorts could not be estimated given the wide variation in reporting.

Data sufficient to distinguish patients in the severe COVID-19 category from the combined category of mild/moderate disease was present in 4 HCT studies (31 patients), 31 SOT studies (501 patients), ten A-CA studies (2,462 patients), and 336 of the patients entered into the CCCR ( Figure 2C ). The estimated pooled prevalence of severe disease was 20·24% (95% CI 16·07-24·94) among P-CA patients, 32·19% (95% CI 12·31-55·07) among HCT patients, 33·16%

(95% CI 19·35-48·43) among A-CA patients, and 42·16 (95% CI 33·52-51·00) among SOT patients.

Despite receiving immunosuppressive therapies, A-CA (n=five) and SOT (n=20) studies reporting WBC indices at time of COVID-19 diagnosis had median leukocyte counts within the normal range and comparable to those reported in the general population with COVID-19 ( Figure 3A) . However, all A-CA studies and all but one 31 SOT study reported low ALC, again comparable to the general population ( Figure 3B ). Similarly, data for P-CA patients showed 51·5% patients (n=565 with leukocyte indices reported) having an ALC<1,000 cells/L. While not reported in a manner permitting calculation of interquartile ranges, six HCT studies 92, 94, [99] [100] [101] reported ALC data with only one 101 showing a median ALC above the lymphopenia range.

Most studies reported elevated inflammatory markers among immunocompromised cohorts. All A-CA (n=three) and SOT (n=19) studies reporting CRP data reported medians above the normal CRP range (Supplemental Figure 2A ). Of these, nine SOT 31, 42, 44, 45, 49, 67, 73, 76, 134 studies and one A-CA study 135 reported median CRP values above the 95% confidence interval for the general population. 128 Of 18 SOT studies and one A-CA study reporting ferritin levels, only one SOT study 63 reported a median ferritin level in the normal range with the remainder of studies having elevated values (Supplemental Figure 2B ). All but one 31 of the SOT studies reporting LDH data (n=16) had median values above the normal range (Supplemental Figure 2C ). In contrast, only one 120 of the three A-CA studies reporting on LDH had a median elevated level and this one just above the cutoff for normal. Only one HCT study reported on inflammatory markers. 101 Among this eight patient cohort the median CRP, ferritin, and LDH were all elevated.

Given the thrombotic complications from COVID-19, D-dimer levels were analyzed (Supplemental Figure 2D) . Among SOT studies, one A-CA study, and one HCT study reporting D-dimer levels, only one of these studies 39 reported a median within the normal range. In all the other studies, the D-dimer level was elevated. Of note, D-dimer was not among the data reported in CCCR data on P-CA patients. Lastly, given its association with COVID-19-associated cytokine release syndrome (CRS) and multisystem inflammatory system in children (MIS-C), IL-6 levels were analyzed (Supplemental Figure 2E) . All eight SOT studies and all four A-CA studies including data on IL-6 showed median IL-6 levels above the normal range with several studies reporting levels above those reported in the general population with COVID-19. No HCT studies reviewed reported on IL-6 levels, which were also not reported in the CCCR for P-CA patients.

Multiple therapies were given to immunocompromised patients with COVID-19 (Table 1) . The most common therapy was hydroxychloroquine. Azithromycin and corticosteroids were the next most commonly utilized therapies. Multiple antiviral agents were trialed among the immunocompromised including remdesivir, lopinavir-ritonavir, darunavir-cobicistat, oseltamivir, umifenovir, ribavirin, favipiravir, and ganciclovir. IL-6 blockade was reported most frequently in the SOT population; and convalescent plasma was rarely trialed.

One common approach to COVID-19 management was modifying baseline immunosuppression or delaying further immunosuppressive therapies (Supplemental Figure 3) . Pooled prevalence estimates for modification/discontinuation by immunosuppressive agent were as follows: 64·7% (95% CI 11·5-100) for mTOR inhibitors, 49·2% (95% CI 32·6-66·0) for calcineurin inhibitors, and 84·5% (95% CI 75·8-91·9) for antimetabolites. Delays in antineoplastic therapies occurred in 56·3% (95% CI 11·4-96·2) of A-CA and 28·4% (95% CI 24·9-32·1) of P-CA patients.

To evaluate severity in a single context that was most uniform across all studies evaluated, we evaluated outcomes data for only hospitalized patients. We calculated the pooled prevalence of critical condition/need for intensive care as well as hospital mortality among hospitalized 

To our knowledge, the current study is the largest meta-analysis analyzing clinical and laboratory data as well as outcomes among different immunocompromised patient populations with COVID-19 and comparing results to a robust general population cohort with COVID-19. As recent meta-analyses have focused exclusively on cancer 136 or SOT patients. 137 Herein, results show differences among the immunocompromised and general population cohorts after COVID-19. First, SOT patients with COVID-19 had more comorbidities (cardiovascular disease, diabetes, and hypertension), dyspnea and required intensive care more often, and had higher mortality despite having similar disease severity versus the general population with COVID-19.

Second, A-CA patients with COVID-19 also had more comorbidities (cardiovascular disease, hypertension) and higher mortality than the general population with COVID-19. Fung and Babik performed the original literature review on immunosuppressed patients with COVID-19, which suggested that SOT and CA patients may be at increased risk for severe disease and adverse outcomes. 138 The current meta-analysis supports these preliminary findings and further enables subgroup analysis of cancer patients by age. Specifically, P-CA have less fever, fatigue, myalgia, cough and dyspnea than their adult counterparts. Additionally, P-CA patients have less hospital-associated mortality than A-CA. Both findings are consistent with recent limited P-CA 139 and more extensive pediatric COVID-19 140 literature, suggesting more mild or asymptomatic infection in pediatric patients.

In a recent prospective, multi-center cohort study involving 482 SOT patients, Kates et al. observed a 28-day mortality rate of 20·5% among inpatients (n=376), which associated with patient age and co-morbidities rather than intensity of immunosuppressive therapy. 141 Outcomes in cancer and transplant patients are improving, given the use of biologic therapies targeting immune response against malignant disease 146 and improvements in the field of transplantation, including enhanced supportive care and use of cellular therapies. 147, 148 Remarkably, these same immunomodulatory and cellular therapies 149 are being applied to patients with severe COVID-19, including pediatric patients. 150 This study has several limitations, including significant study heterogeneity largely due to inherent differences among the immunocompromised patient populations but also differences in data collection among studies. Secondly, due to sample size limitations, subset analyses like effect of therapeutic agent or graft type on outcome could not be performed. Thirdly, the followup period varied significantly across studies, affecting outcomes like mortality. Lastly, the study could not perform univariable and multivariable analyses for constructing risk models for severe COVID-19 disease.

Notwithstanding these limitations, the work is the first systematic review summarizing COVID-19 in distinct immunocompromised patient populations and comparing data with the general population. In so doing, immunocompromised patients were found to have more comorbidities than the general population, have worse outcomes among patients requiring hospitalization for COVID-19 compared to the general population, and experience alterations in the management of their primary disease that may place them at risk for worse outcomes. Future study directions must focus on reporting identified gaps presented herein and ensuring uniform data capture.

The authors report no conflicts of interest relevant to the published work. Pooled prevalence estimates of need for intensive care and mortality were calculated from patient data exclusively on hospitalized immunocompromised patients from those studies where such data was explicitly reported. The pooled prevalence is depicted as a filled circle with the bar representing 95% confidence intervals. Data from two large studies 130, 131 (total n=11,721) of hospitalized COVID-19 patients from the general population were utilized to calculate comparable pooled prevalence estimates (vertical hatched line) and 95% confidence intervals (respective gray bars). 

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