key: cord-0876297-jyedcucf
authors: Marra, Alexandre R.; Kobayashi, Takaaki; Suzuki, Hiroyuki; Alsuhaibani, Mohammed; Tofaneto, Bruna Marques; Bariani, Luigi Makowski; Auler, Mariana de Amorim; Salinas, Jorge L.; Edmond, Michael B.; Doll, Michelle; Kutner, José Mauro; Pinho, João Renato Rebello; Rizzo, Luiz Vicente; Miraglia, João Luiz; Schweizer, Marin L.
title: Short-term effectiveness of COVID-19 vaccines in immunocompromised patients: A systematic literature review and meta-analysis
date: 2022-01-01
journal: J Infect
DOI: 10.1016/j.jinf.2021.12.035
sha: f96258eb8e72f2ade746892166f3e27a6083c611
doc_id: 876297
cord_uid: jyedcucf

OBJECTIVES: We aimed to assess the short-term effectiveness of COVID-19 vaccines among immunocompromised patients to prevent laboratory-confirmed symptomatic COVID-19 infection. METHODS: Systematic review and meta-analysis. We calculated the pooled diagnostic odds ratio [DOR] (95% CI) for COVID-19 infection between immunocompromised patients and healthy people or those with stable chronic medical conditions. VE was estimated as 100% x (1-DOR). We also investigated the rates of developing anti-SARS-CoV-2 spike protein IgG between the 2 groups. RESULTS: Twenty studies evaluating COVID-19 vaccine response, and four studies evaluating VE were included in the meta-analysis. The pooled DOR for symptomatic COVID-19 infection in immunocompromised patients was 0.296 (95% CI: 0.108–0.811) with an estimated VE of 70.4% (95% CI: 18.9%- 89.2%). When stratified by diagnosis, IgG antibody levels were much higher in the control group compared to immunocompromised patients with solid organ transplant (pOR 232.3; 95% Cl: 66.98–806.03), malignant diseases (pOR 42.0, 95% Cl: 11.68–151.03), and inflammatory rheumatic diseases (pOR 19.06; 95% Cl: 5.00–72.62). CONCLUSIONS: We found COVID-19 mRNA vaccines were effective against symptomatic COVID-19 among the immunocompromised patients but had lower VE compared to the controls. Further research is needed to understand the discordance between antibody production and protection against symptomatic COVID-19 infection.

The first coronavirus disease vaccine was authorized by the U.S. Food and Drug Administration (FDA) on December 11, 2020 for prevention of severe illness or death. That mRNA vaccine demonstrated an efficacy of 95% (1) and humoral and cellular responses were triggered within 1 week after the second dose (2) . Subsequently, eight more vaccines have been authorized after phase III trials (3) .

Previous studies evaluated vaccine effectiveness (VE) among individuals who were healthy or had stable chronic medical conditions (1) . Since immunocompromised patients were excluded from trials conducted early in this pandemic, there is less data on immunocompromised patients compared with other patient populations. Due to growing concern over a poor response to vaccination among immunocompromised patients who are particularly at risk for severe disease, and some evidence for the benefit of booster doses (4) the U.S. FDA gave emergency use authorization for an additional dose of COVID-19 vaccines for immunocompromised people on August 12, 2021 (5) .

Recently, some studies provided real-world data on VE in people with immunocompromising conditions (6, 7) . Other studies evaluated the humoral immune response among these patients (8) . Studies suggested that immunocompromised patients who received COVID-19 vaccines might not develop high neutralizing antibody titers or be as protected against severe COVID-19 outcomes as are immunocompetent patients (9, 10) . Vaccine responsiveness in patients who were receiving an immunosuppressor drug therapy exhibited impaired serological immune responses (9, 11) . Though there is growing evidence that VE and immune response among immunocompromised patients seem lower than in healthy people, limited data are available (4, 6, 8) . Given higher complication and mortality rates from COVID-19 (12) , it is important to quantify vaccine effectiveness and assess whether this group is capable of producing neutralizing antibodies.

We aimed to review the literature on the impact of COVID-19 vaccination on neutralizing antibodies and the short-term effectiveness of COVID-19 vaccines among immunocompromised patients to prevent laboratory-confirmed symptomatic COVID-19 infection.

This review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement (13) and the Meta-analysis of Observational Studies in Epidemiology (MOOSE) guidelines (14) . This study was registered on Prospero (https://www.crd.york.ac.uk/PROSPERO/) on 6 Randomized clinical trials (phase III), commentaries, studies with overlapping patients, studies in pediatric populations, and studies from non-peer reviewed studies (e.g., MedRxiv) were excluded. Studies in which there was no comparison between vaccinated immunocompromised patients and vaccinated control groups, evaluating just one dose of COVID-19 vaccine, and those in which no VE data were published were also excluded.

We performed literature searches in PubMed, Cumulative Index to Nursing and Allied Health (CINAHL), Embase (Elsevier Platform), Cochrane Central Register of Controlled Trials, Scopus, and Web of Science. The entire search strategy is described in Supplementary Appendix 1. We reviewed the reference lists of retrieved articles to identify studies that were not identified from the preliminary literature searches. After applying exclusion criteria, we reviewed 71 papers, 33 of which met the inclusion criteria and were included in the systematic literature review [ Figure 1 ].

Titles and abstracts of all articles were screened to assess whether they met inclusion criteria. The reviewers (ARM, TK, HS, MAA, BMT, LMB, and MAA) abstracted data for each article. Reviewers resolved disagreements by consensus.

The reviewers abstracted data on study design, population and setting, study period (weeks or months), number of patients (immunocompromised vs. the control group), the total number of participants who produced neutralizing antibodies after one or two doses between immunocompromised vs. the control group, the mean or the median antibody levels after one or two doses among immunocompromised and the control groups, humoral and cellular immunity studies, and the immunosuppressive drugs used in each study. The FDA recommends defining the COVID-19 endpoint as virologically confirmed SARS-CoV-2 infection accompanied by symptoms (16) . For that reason, we have defined the primary outcome as symptomatic COVID-19 infection.

Risk of bias was assessed using the Downs and Black scale (17). Reviewers followed all questions from this scale as written except for question #27 (a single item on the Power subscale, scored 0 to 5), which was changed to a yes or no. For the analysis, we classified the studies as good (19-23 of 28 possible points), or fair (14-18 points of 28 possible points) quality. Two authors performed component quality analysis independently, reviewed all inconsistent assessments, and resolved disagreements by consensus (18) .

To meta-analyze the extracted data, COVID-19 vaccine response was assessed using a randomeffects model to estimate pooled odds ratios and 95% confidence intervals with weights as described by DerSimonian and Laird (19) . We performed stratified analyses of the associations between anti-SARS-CoV-2 spike protein IgG production after two doses of COVID-19 vaccine between immunocompromised patients and the control group. We also performed stratified analyses among studies in patients with solid organ transplants, with malignancy or with inflammatory rheumatic diseases, respectively, in studies that evaluated neutralizing antibodies after COVID-19 vaccine, and in studies classified as good vs. fair per the Downs and Black score. In our stratified analyses we did not include studies that did not report the absolute number of patients that produced anti-SARS-CoV-2 spike protein IgG after the second vaccine dose. We did not include in our metaanalysis studies where only mean or the median antibody levels were reported. Heterogeneity between studies was evaluated with I 2 estimation and the Cochran Q statistic test. We used the Cochrane Review Manager version 5.3.

We also calculated the pooled diagnostic odds ratio [DOR] (95% confidence interval) for symptomatic COVID-19 between vaccinated immunocompromised patients and vaccinated healthy controls or other vaccinated controls with similar clinical conditions. VE was estimated as 100% x (1-DOR). We performed statistical analysis using R version 4.1.0 with mada package version 0.5.4 (20) . Analogous to the metaanalysis of the odds ratio methods for the DOR, an estimator of random effects model following the approach of DerSimonian and Laird is provided by mada package (20) . For the meta-analysis of estimates of COVID-19 VE, we used a bivariate random effects model, adopting a similar concept of calculating diagnostic accuracy, which enables simultaneous pooling of sensitivity and specificity with mixed-effect linear modeling while allowing for the trade-off between them (21, 22) . Heterogeneity between studies was also evaluated with I 2 estimation and the Cochran Q statistic test. Publication bias was assessed using funnel plots.

Thirty-three studies met the inclusion criteria and were included in the final review ( Figure 1 ). All of these studies were non-randomized, of which, twenty-seven were prospective cohort studies (24, 25, 27, 28, 30-37, 39, 41-54) , and six were retrospective cohort studies (23, 26, 29, 38, 40, 55) . The majority of them (32 studies) evaluated the Pfizer/BioNTech mRNA COVID-19 vaccine (53) (54) (55) . Six of these studies also analyzed the Moderna mRNA COVID-19 vaccine (28, 32, 33, 40, 53, 55) and another also analyzed the AstraZeneca COVID-19 vaccine (42) . Just one study evaluated the Coronavac COVID-19 vaccine (52) . None of the studies evaluated the VE for the Johnson & Johnson/Janssen vaccine.

The majority of the studies included in our review were conducted in Israel (nine studies) (23, 27, 29, 31, 34, 37, 38, 47, 48) , following by the United States (six studies), (33, 35, 40, (53) (54) (55) , Germany (five studies) (32, 41, (49) (50) (51) , France (four studies) (25, 26, 30, 43) , Italy (two studies) (39, 45) , the United Kingdom (two studies) (42, 46) , and Czech Republic (36), Denmark (24) , Lithuania (44) , Spain (28) , and Turkey (52) with one study each. All studies were performed between December 2020 and May 2021 . Eleven studies evaluated solid organ transplant recipients (26, 30, 34, 36, 41, 45, (47) (48) (49) (50) (51) , being two studies of them evaluated hemodialysis patients (26, 30) . Eight studies evaluated patients with malignant diseases (25, 33, 37-39, 42, 44, 46) , six studies evaluated patients with inflammatory rheumatic diseases (24, 27, 31, 32, 35, 52) , two studies evaluated patients with inflammatory bowel diseases (40, 55) , two studies evaluated patients with chronic kidney failure on hemodialysis (28, 43) , one study evaluated patients with multiple sclerosis (23) , and one study evaluated HIV patients (54) . The definition of immunocompromised condition was not reported in two studies (29, 53) .

Studies varied on their reporting of characteristics of the serological tests, including when they were performed, cutoff levels for antibody positivity, and the type of serological test analysis performed (Supplementary Appendix 2). Eight studies did not report the cut-off level for their specific assay (29, 32, 36, 40, 46, 47, 49, 53) . Three studies did not use serological tests to determine vaccine effectiveness (29, 40, 53) .

The cellular immunity investigation was performed in 10 studies with different approaches (26, 28, 35, 36, 45, 46, (49) (50) (51) 54) (Supplementary Appendix 2) . Twenty-three studies did not report any cellular immune investigation (23-25, 27, 29-34, 37-44, 47, 48, 52, 53, 55) .

Four studies evaluated the variants of concerns (VOC) in some of patients' samples (44, 46, 53, 54) .

One study found that HIV patients and the healthy control group had similar levels of neutralizing antibodies to the vaccine strain spike protein and spike proteins from VOC including, alpha (B.1.1.7), beta (B.1.351), and gamma (P.1) strains (54) . One study detected neutralization assays of VOC alpha lineage (46) . Another one studied seven patients with hematological malignancies with breakthrough infection detecting mutations of the alpha (B.1.1.7 strain) variant (44) . Only one study performed genomic surveillance detecting the SARS-CoV-2 (alpha), beta, and gamma variants, where alpha variant was the most common lineage (53) . The majority of the included studies did not perform genomic surveillance (23-43, 45, 47-52, 55) .

Regarding the quality assessment scores of the 33 included studies, more than half of the studies (22 studies) were considered good (19-23 of 28 possible points) per the Downs and Black quality tool (24, 27-29, 31-38, 40, 41, 43, 44, 46, 48, 51-53, 55) . Eleven studies were considered fair (14-18 points) (23, 25, 26, 30, 39, 42, 45, 47, 49, 50, 54) , and no study was considered poor quality (<14 points).

Among 33 studies identified for the systematic literature review, 30 studies evaluated the COVID-19

vaccine response with anti-SARS-CoV-2 spike protein IgG after the second dose (23-28, 30-35, 37-39, 41-55) .

Of them, 10 studies reported only mean or median of anti-SARS-CoV-2 spike protein IgG, but they did not report positive rates (24, 26-28, 32, 36, 39, 44, 50, 54) . Twenty studies reported positive rates of anti-SARS-CoV-2 spike protein IgG with a total of 2,219 immunocompromised patients, and were included in the metaanalysis (23, 25, 30, 31, 33-35, 37, 38, 41-43, 45-49, 51, 52, 55) . The positive rate ranged from 0% to 100%. 

Based on studies evaluating short-term VE between December 2020 and May 2021, this systematic literature review and meta-analysis showed that COVID-19 vaccines (primarily the mRNA COVID-19 vaccines) decrease symptomatic COVID-19 infection with a VE of 70.4% in immunocompromised patients. This number was lower compared to VE in the general population reported in the randomized trials (1, 56) in a noncontrolled setting (57) , and also in a recent meta-analysis among healthcare workers (HCWs) (58) . We also found that a wide range of anti-SARS-CoV-2 spike protein IgG development has been reported after two doses of COVID-19 vaccines among those immunocompromised and the rate of response was significantly lower compared to the control group in these studies.

There is no test to quantify the level of immunosuppression in an immunocompromised patient.

However in our meta-analysis we were able to identify that immunocompromised patients with a variety of vaccine in immunocompromised patients as well as other protective measures (facial masks and social distancing) until more data on short-and long-term vaccine effectiveness is obtained (57, 58) . Prior studies demonstrated chronic kidney disease patients undergoing hemodialysis have more IgG antibody levels after receiving COVID-19 vaccines than kidney transplant recipients (26, 30) . Also, a recent European cohort study of patients with hemato-oncological diseases and a control group of HCWs suggested that patients with cancer developed lower antibody, and those receiving chemotherapy and B cell-targeting agents showed a particularly impaired serological response (9) . This could suggest that the immunosuppressant therapy may be a critical factor implicated in this lack of humoral response.

For the humoral response, the most utilized and reported method was IgG antibody titers. These could be total antibody levels or levels against specific structural proteins, such as spike (S) or membrane proteins of SARS-CoV-2. The antibody response can be reported as positive or negative based on the manufacturer's criteria, actual titers, or relative titers as ratio to an internal control (63) . Measurement of neutralizing capability against live viruses or pseudo-viruses is more reflective of the robustness of humoral response because it directly measures the capability to suppress viral growth (64) . However, the U.S. FDA does not recommend antibody testing for SARS-CoV-2 to determine immunity or protection from COVID-19, especially among those who are vaccinated (65) . In fact, our study showed extremely variable level of antibody response ranging from 0 to 100% among immunocompromised patients, yet the VE was moderately high at 70%. Further research is needed to understand the discordance between antibody production and protection against symptomatic COVID-19 infection.

Our study had several limitations. First, we only included observational studies for the meta-analysis, which are subject to multiple biases (66) . However, this is the most common type of study in the infection prevention literature (66) . Second, since we estimated the VE based on only short-term durations, we could not evaluate the long term VE or need for a third vaccine dose. One recent study published after our systematic search ended evaluated the long term VE among those immunocompromised and reported the effectiveness of mRNA vaccination against COVID-19 hospitalization was lower (77%) among immunocompromised individuals than among immunocompetent individuals (90%) over nine months (10) . There is a need for longerterm observational studies to assess sustained immune response and VE. Third, each study adopted different serological tests to quantify antibody response to SARS-CoV-2 after COVID-19 vaccine among immunocompromised patients . Fourth, we do not have any data to evaluate how good enough were cellular immunity to prevent severe disease or mortality among immunocompromised populations. This could represent that many of the studies reviewed were challenging due to lack of information regarding the intensity of immunosuppression or capture of the incidence of COVID-19 outside the hospital. Fifth, our systematic review has not included studies that detected the delta variant, which contributed to the majority of recent breakthrough infections around the world (67, 68) . We need more studies on the SARS-CoV-2 variants of concerns (VOC) that have multiple spike protein mutations and appear to be more infectious or cause more disease than other circulating SARS-CoV-2 variants (69). One recent study performed genomic surveillance detecting the new SARS-CoV-2 delta variant, alpha variant, and other variants (70) . It was not included in our systematic review because there is an overlapping of patients in this study with another study (53) , and we were unable to extract data for the meta-analysis to calculate VE for symptomatic COVID-19 infection. Sixth, different definitions were used in different studies for immunocompromising conditions. There may also be diagnostic overlap since immunocompromised patients can have multiple comorbidities. Finally, the results of our meta-analysis should be interpreted with caution, particularly since only four studies were included to calculate the COVID-19 VE among immunocompromised patients. Additionally, there was considerable heterogeneity in the identified studies, and there was not enough data to run additional stratified analysis for asymptomatic COVID-19, or COVID-19 breakthrough infections.

We found that the COVID-19 mRNA vaccines were moderately effective against symptomatic COVID- 

This study was not funded.

All authors report no conflict of interest relevant to this article. 

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*We have opted to include in our meta-analysis Tenforde 2021 CID [50] because in Tenforde 2021 MMWR study [67] there are no raw numbers to perform the vaccine effectiveness for immunocompromised patients