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Mayo Clinic Proceedings: Innovations, Quality & Outcomes logoLink to Mayo Clinic Proceedings: Innovations, Quality & Outcomes
. 2023 Oct 10;7(5):499–513. doi: 10.1016/j.mayocpiqo.2023.09.001

Rates Among Hospitalized Patients With COVID-19 Treated With Convalescent Plasma: A Systematic Review and Meta-Analysis

Jonathon W Senefeld a,b,∗, Ellen K Gorman a, Patrick W Johnson i, M Erin Moir k, Stephen A Klassen l, Rickey E Carter i, Nigel S Paneth m, David J Sullivan n, Olaf H Morkeberg a, R Scott Wright d,d, DeLisa Fairweather j, Katelyn A Bruno j,o, Shmuel Shoham p, Evan M Bloch q, Daniele Focosi r, Jeffrey P Henderson s,t, Justin E Juskewitch e, Liise-Anne Pirofski v, Brenda J Grossman u, Aaron AR Tobian q, Massimo Franchini w, Ravindra Ganesh f, Ryan T Hurt f, Neil E Kay g,h, Sameer A Parikh g, Sarah E Baker a, Zachary A Buchholtz a, Matthew R Buras x, Andrew J Clayburn a, Joshua J Dennis a, Juan C Diaz Soto a, Vitaly Herasevich a, Allan M Klompas a, Katie L Kunze x, Kathryn F Larson c, John R Mills e, Riley J Regimbal a, Juan G Ripoll a, Matthew A Sexton a, John RA Shepherd a, James R Stubbs e, Elitza S Theel e, Camille M van Buskirk e, Noud van Helmond a, Matthew NP Vogt a, Emily R Whelan j, Chad C Wiggins a, Jeffrey L Winters e, Arturo Casadevall n, Michael J Joyner a
PMCID: PMC10582279  PMID: 37859995

Abstract

Objective

To examine the association of COVID-19 convalescent plasma transfusion with mortality and the differences between subgroups in hospitalized patients with COVID-19.

Patients and Methods

On October 26, 2022, a systematic search was performed for clinical studies of COVID-19 convalescent plasma in the literature from January 1, 2020, to October 26, 2022. Randomized clinical trials and matched cohort studies investigating COVID-19 convalescent plasma transfusion compared with standard of care treatment or placebo among hospitalized patients with confirmed COVID-19 were included. The electronic search yielded 3841 unique records, of which 744 were considered for full-text screening. The selection process was performed independently by a panel of 5 reviewers. The study followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Data were extracted by 5 independent reviewers in duplicate and pooled using an inverse-variance random effects model. The prespecified end point was all-cause mortality during hospitalization.

Results

Thirty-nine randomized clinical trials enrolling 21,529 participants and 70 matched cohort studies enrolling 50,160 participants were included in the systematic review. Separate meta-analyses reported that transfusion of COVID-19 convalescent plasma was associated with a decrease in mortality compared with the control cohort for both randomized clinical trials (odds ratio [OR], 0.87; 95% CI, 0.76-1.00) and matched cohort studies (OR, 0.76; 95% CI, 0.66-0.88). The meta-analysis of subgroups revealed 2 important findings. First, treatment with convalescent plasma containing high antibody levels was associated with a decrease in mortality compared with convalescent plasma containing low antibody levels (OR, 0.85; 95% CI, 0.73 to 0.99). Second, earlier treatment with COVID-19 convalescent plasma was associated with a decrease in mortality compared with the later treatment cohort (OR, 0.63; 95% CI, 0.48 to 0.82).

Conclusion

During COVID-19 convalescent plasma use was associated with a 13% reduced risk of mortality, implying a mortality benefit for hospitalized patients with COVID-19, particularly those treated with convalescent plasma containing high antibody levels treated earlier in the disease course.

The COVID-19 pandemic created a humanitarian crisis that prompted an expeditious search for safe and effective COVID-19 therapies. Before identifying effective antispike monoclonal antibodies and small molecule antivirals, COVID-19 convalescent plasma was proposed as a safe treatment with a promising efficacy profile in early reports.1, 2, 3 More recently, as new SARS-CoV-2 variants emerged and evaded antispike monoclonal antibodies,4,5 interest has been renewed in understanding the clinical efficacy of COVID-19 convalescent plasma,6 particularly among patients who are immunocompromised.7 Although COVID-19 convalescent plasma has been widely available and used to treat over half a million patients with COVID-19,8 uncertainty remains about the utility of COVID-19 convalescent plasma and its association with mortality because of heterogenous findings from individual studies.9 Heterogeneity in clinical studies is likely due to several key factors: biological diversity of COVID-19 convalescent plasma, evolving and nonstandard treatment protocols, and a wide spectrum of clinical use of COVID-19 convalescent plasma, from postexposure prophylaxis to therapy of last resort in patients with multiorgan failure. In this framework, many different approaches have been used to study the mortality of patients with COVID-19 treated with COVID-19 convalescent plasma, including randomized clinical trials (RCTs),10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48 real-time pooling of individual patient data from RCTs,6,49 and meta-analyses.41,50, 51, 52, 53 The present work was performed to provide an updated, high-quality systematic review and meta-analysis on the use of COVID-19 convalescent plasma.

This systematic review and meta-analysis aimed to evaluate the association of COVID-19 convalescent plasma with mortality among hospitalized patients with COVID-19 by pooling data from RCTs and matched cohort studies. Moreover, prespecified analyses aimed to determine if the potential association between COVID-19 convalescent plasma and mortality benefit differs across patient subgroups on the basis of anti-SARS-CoV-2 antibody levels within COVID-19 convalescent plasma and the timing of the convalescent plasma transfusion in relation to the disease course.54 By integrating information from many studies and lines of evidence, we hope that this work provides new insights, clarifies ambiguous areas, and removes biases from the scientific corpus.55

Methods

This systematic review and meta-analysis followed the recommendations in the Cochrane Handbook for Systematic Review of Interventions56 and reported findings according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses reporting guidelines. The study protocol has been registered in the International Prospective Register of Systematic Reviews (CRD42022316321); all changes to the protocol are reported in the Methods section. In accordance with the Code of Federal Regulations, 45 CFR 46.102, this study was exempt from obtaining institutional review board approval from Mayo Clinic and the requirement to obtain informed patient consent because it is a secondary use of publicly available data sets.

Eligibility Criteria

Eligible patients were hospitalized with COVID-19. The intervention investigated was transfusion with COVID-19 convalescent plasma of any dosage. The control group was treated with standard of care according to local treatment guidelines, with or without a placebo. The primary outcome was all-cause mortality during hospitalization. Randomized clinical trials and matched cohort studies were eligible for all analyses. For subgroup analyses, where the focus is on differences among patients treated with COVID-19 convalescent plasma, case series were also eligible.

Information Sources

On October 26, 2022, PubMed, MEDLINE, Google Scholar, and medRiv were searched for eligible studies published beginning with January 1, 2020—approximating the origins of the COVID-19 pandemic. Keywords used in the search included ([convalescent plasma] or [convalescent serum]) COVID-19 (and medical subject headings).

Selection and Data Collection Processes

Both the selection process and data collection process were performed in duplicate and independently by 2 reviewers from a cohort of 5 potential reviewers (J.W.S., E.K.G., M.E.M., S.A.K., and O.H.M.), and all data were independently verified by review from a third reviewer. Disagreements were discussed until consensus. Data abstraction was performed using a standardized data abstraction form. Abstracted data included patient demographic characteristics (sample size, age, sex, and need for mechanical ventilation at the time of COVID-19 convalescent plasma transfusion) and COVID-19 convalescent plasma transfusion characteristics (volume transfused, antibody level, and time to transfusion in relation to disease course) as available. Data were abstracted corresponding to the latest available follow-up time for mortality. Further information on the selection process is presented in Figure 1.

Figure 1.

Figure 1

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PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flow diagram.

Study Risk of Bias Assessment

A risk of bias assessment was conducted using the Cochrane risk of bias 2.0 tool for RCTs57,58 and the Newcastle-Ottawa Scale for matched cohort studies. Two reviewers from a cohort of 3 potential reviewers (J.W.S., E.K.G., and S.A.K.) applied the risk of bias assessment independently and it was verified by a third reviewer. Discrepancies were discussed until a consensus was reached.

Statistical Analyses

For the primary, dichotomous outcome of mortality, we performed a meta-analysis using a random effects model. We extracted raw data on mortality events and the number of patients in each group. For each study, we compared the observed number of deaths among patients transfused with COVID-19 convalescent plasma with the expected number if all patients were at equal risk using standard formulas for 2×2 contingency tables. Trial results were combined and weighted using an inverse-variance model. Analyses were done using Comprehensive Meta-analysis software (CMA 2.0, Biostat). Results are reported with 95% CIs, statistical significance was set at α=.05, and all tests were 2-tailed.

Primary meta-analyses were performed separately for RCTs and matched cohort studies. We performed prespecified subgroup analyses, including a subgroup analysis on the basis of the timing of convalescent plasma transfusion (early vs late treatment) in relation to the COVID-19 disease course and a subgroup analysis on the basis of antibody concentration in the transfused COVID-19 convalescent plasma (high vs low antibody levels).

In addition, an exploratory meta-analysis was performed on hospitalization rates among outpatients with recent SARS-CoV-2 exposure or infection.

Results

Study Selection and Characteristics

The process of study selection is represented in the Preferred Reporting Items for Systematic Reviews and Meta-analyses flow diagram (Figure 1). Thirty-nine RCTs10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48 enrolling 21,529 participants and 70 matched cohort studies2,59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83, 84, 85, 86, 87, 88, 89, 90, 91, 92, 93, 94, 95, 96, 97, 98, 99, 100, 101, 102, 103, 104, 105, 106, 107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117, 118, 119, 120, 121, 122, 123, 124, 125, 126, 127 enrolling 50,160 participants were included in the primary analyses. Although controlled studies were the focus of this systematic review and meta-analysis, secondary analyses on COVID-19 convalescent plasma antibody levels and timing of COVID-19 convalescent plasma transfusion encompass findings from case series, as delineated below.

Risk Assessment

The results of the risk of bias assessment for RCTs and matched cohort studies are presented in Supplemental Tables 2 and 3, respectively, available online at http://www.mcpiqojournal.org. Because our analyses primarily included controlled trials and focused on a discrete, dichotomous outcome that is unlikely to be influenced by the implicit biases of research personnel (all-cause mortality), many studies were determined to have low risk of bias. Matched cohort studies were associated with higher risk of bias because of the open-label trial design.

Association Between Convalescent Plasma Transfusion and Mortality in Hospitalized Patients with COVID-19

Key findings of the primary meta-analysis of 39 RCTs including 11,303 patients treated with COVID-19 convalescent plasma and 10,226 patients treated with usual care (controls), are displayed in Figure 2. Treatment with COVID-19 convalescent plasma was associated with a 13% reduced risk in mortality rates compared with usual care, with a pooled risk ratio estimate of 0.87 (95% CI, 0.76-1.00).

Figure 2.

Figure 2

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Forest plot of mortality among randomized clinical trials.

The clinical benefit associated with COVID-19 convalescent plasma observed in 39 RCTs was also supported by a meta-analysis of 70 matched cohort studies, which included 14,541 patients treated with COVID-19 convalescent plasma and 35,619 patients treated with usual care (controls). In this meta-analysis of matched cohort studies, treatment with COVID-19 convalescent plasma was associated with a 23% reduced risk in mortality rates compared with usual care, with a pooled risk ratio estimate of 0.76 (95% CI, 0.66-0.88). A forest plot associated with these findings is displayed in Supplemental Figure 1, available online at http://www.mcpiqojournal.org. Although there was heterogeneity between individual studies, there was a high level of concordance between these 2 separate meta-analyses.

Exploratory Analyses of Outpatient COVID-19 Convalescent Plasma

Six RCTs128, 129, 130, 131, 132, 133 enrolling 2824 participants were included in an exploratory analysis of hospitalization or mortality rates among outpatients with recent SARS-CoV-2 exposure or infection. In this meta-analysis, treatment with COVID-19 convalescent plasma among outpatients was associated with a 35% decrease in hospitalization rate, with a pooled risk ratio estimate of 0.65 (95% CI, 0.45-0.94). Results of this exploratory meta-analysis are shown in the forest plot in Figure 3. However, there was no apparent mortality benefit associated with convalescent plasma among outpatients, with a pooled risk ratio estimate of 0.60 (95% CI, 0.16-2.28; Supplemental Figure 2, available online at http://www.mcpiqojournal.org.)

Figure 3.

Figure 3

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Forest plot of hospitalization among outpatients with recent SARS-CoV-2 exposure or infection in randomized clinical trials.

Subgroup Analyses

COVID-19 Convalescent Plasma Antibody Levels

Among patients treated with COVID-19 convalescent plasma, receipt of convalescent plasma with higher levels of antibodies has been suggested to be associated with reduced mortality.20,54 Thus, heterogeneity of antibody levels in the COVID-19 convalescent plasma used to treat patients may affect the mortality rates reported. Hence, we examined within-study mortality rates among patients treated with convalescent plasma containing high or low antibody levels. Because several assays were authorized for use in the manufacture of high antibody-titer convalescent plasma and the cutpoints used to qualify high antibody-titer convalescent plasma have changed over time, we used study-defined cutpoints to define high and low antibody levels. Information on assay systems and cutpoints used to delineate high and low antibody levels are provided in Supplemental Table 4, available online at http://www.mcpiqojournal.org.

In this framework, 3 matched cohort studies98,109,114 enrolling 330 participants and 12 case series54,134, 135, 136, 137, 138, 139, 140, 141, 142, 143, 144 enrolling 29,361 participants were included in this subgroup analysis. In this subgroup meta-analysis, treatment with COVID-19 convalescent plasma containing high antibody levels was associated with a 15% decrease in mortality rates compared with convalescent plasma containing low antibody levels, with a pooled risk ratio estimate of 0.85 (95% CI, 0.73-0.99). The results of this subgroup meta-analysis are shown in the forest plot in Figure 4.

Figure 4.

Figure 4

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Forest plot of mortality among studies investigating COVID-19 convalescent plasma containing high compared with low antibody levels.

Timing of COVID-19 convalescent plasma transfusion

Among hospitalized patients transfused with COVID-19 convalescent plasma, transfusion earlier in the COVID-19 disease course has been suggested to be associated with reduced mortality,52,54,72 thus, heterogeneity of the time between COVID-19 diagnosis and convalescent plasma transfusion may affect mortality rates. Because there was no standard to define ‘early treatment’ and individual studies used diverse criteria to define ‘early treatment’, we used study-defined cutpoints to delineate early and late treatment with COVID-19 convalescent plasma. Information on cutpoints used to define earlier and later treatment with COVID-19 convalescent plasma are provided in Supplemental Table 5, available online at http://www.mcpiqojournal.org.

In this context, we examined within-study mortality rates among patients treated with convalescent plasma earlier compared with those treated later in the COVID-19 disease course. This subgroup analysis examined 26 studies, including 2 RCTs14,41 enrolling 5990 participants, 7 matched cohort studies69,72,97,101,109, 110, 111 enrolling 1928 participants, and 17 case series136, 137, 138,140,145, 146, 147, 148, 149, 150, 151, 152, 153, 154, 155, 156, 157 enrolling 10,530 participants. In this subgroup meta-analysis, treatment with convalescent plasma earlier in the COVID-19 disease course was associated with a 37% decrease in mortality rates compared with treatment later in the disease course, with a pooled risk ratio estimate of 0.63 (95% CI, 0.48-0.82). The results of this subgroup meta-analysis are shown in the forest plot in Figure 5.

Figure 5.

Figure 5

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Forest plot of mortality among studies investigating earlier compared with later transfusion of COVID-19 convalescent plasma.

Case Series and Reports

In the United States and many other countries, the regulatory framework during the COVID-19 pandemic enabled broad access to COVID-19 convalescent plasma.158 In this context, a large number of single-arm studies evaluated the risk of death from COVID-19 after transfusion with convalescent plasma, including over 300 case series or case reports. The case series and case reports treated 135,949 participants with COVID-19 convalescent plasma, and mortality was observed in 33,771 participants (∼25% mortality rate). Study level data are provided in Supplementary Table 6, and references associated with these case series and case reports are provided in the supplementary references.

Discussion

This systematic review and meta-analysis of 39 RCTs and 70 matched cohort studies of the use of COVID-19 convalescent plasma for hospitalized patients with COVID-19 provides new insights into the therapeutic use of convalescent plasma and removes biases from the scientific and clinical literature. This meta-analysis found that convalescent plasma was associated with a clinically meaningful mortality benefit among hospitalized patients with COVID-19. However, given the large diversity of the included trials and the heterogeneity of findings, the results must be analyzed and interpreted critically.

Overall, COVID-19 convalescent plasma transfusion was associated with a 13% decrease in mortality rates compared with the (usual care) control group. Subgroup analyses revealed that patients treated with high-titer plasma and patients treated earlier in the course of the disease benefited more from COVID-19 convalescent plasma transfusion than patients treated with lower-titer plasma or patients treated later in the course of the disease. Exploratory analyses also found that transfusion of COVID-19 convalescent plasma among outpatients was associated with a 35% decrease in hospitalization rates compared with the control group—a finding that is consistent with pooled individual patient data.159 Our finding that convalescent plasma transfusion reduced mortality is consistent with the epidemiologic data showing an inverse correlation between plasma use and COVID-19 death in the United States.8

Although data were directionally consistent when pooling RCTs and matched cohort studies, findings of individual trials were heterogeneous. This heterogeneity between trials is likely associated with several factors. First, clinical heterogeneity may be on the basis of patient characteristics at the time of COVID-19 convalescent plasma therapy. It is important to consider COVID-19 disease severity, which is directly related to higher odds of death. Among studies in which the patients had more severe disease, mortality was higher, and there was often no clinical benefit associated with COVID-19 convalescent plasma transfusion.160 This meta-analysis found that treatment with COVID-19 convalescent plasma earlier in the course of the disease was associated with a 37% decrease in mortality rates. Thus, treatment later in the course of the disease may not confer a mortality benefit unless the patients are immunocompromised.161

Second, clinical heterogeneity may result from differences in the COVID-19 convalescent plasma intervention itself, particularly the antibody content and geographic provenance of plasma supplies.162 Several assays are authorized for use in the manufacture of high antibody-titer convalescent plasma, and there are established, assay-specific cutpoints used to define high antibody-titer convalescent plasma. However, there is discordance between assays, and the cutpoints to define high antibody-titer convalescent plasma are not directly comparable across assays.163 In addition, the cutpoints used to qualify high antibody-titer convalescent plasma have changed over time, and generally, the required antibody content has increased. In this context, the discordance between assays and changing clinical guidelines may have contributed to the heterogeneity of individual trial findings. This meta-analysis found that treatment with high-titer convalescent plasma was associated with a 15% decrease in mortality rates, and treatment with low-titer convalescent plasma may not confer a clinically meaningful mortality benefit.

Critical reporting and sufficient analyses are crucial when it comes to investigating heterogeneity of meta-analyses in systematic reviews. Failure to fully reflect heterogeneity of results may lead to misinterpretations, incorrect assumptions, and incorrect and potentially harmful clinical recommendations. In this framework, this meta-analysis may provide new insights into the therapeutic use of convalescent plasma. Although this meta-analysis revealed that convalescent plasma was associated with a clinically meaningful overall mortality benefit among hospitalized patients with COVID-19, convalescent plasma is not a panacea because it is a nonstandardized therapy that requires early use for efficacy. COVID-19 convalescent plasma may be unlikely to confer a mortality benefit among patients treated with low antibody-titer convalescent plasma later in the COVID-19 disease course. The finding that COVID-19 convalescent plasma was associated with reduced mortality is consistent with the historical experience of the 1918 pandemic, where convalescent serum therapy was associated with reduced mortality.164

Limitations

This systematic review and meta-analysis has several limitations. First, the empirical and clinical studies were associated with biological diversity and heterogeneous comparator groups. Key factors were continuously evolving during the pandemic, including the pathogen of interest (SARS-CoV-2), contemporary treatment strategies for the disease of interest (COVID-19), and antibody content of the treatment of interest (COVID-19 convalescent plasma). In this context, we believe the high level of concordance among study outcomes despite the biological heterogeneity between studies offers compelling evidence for the therapeutic value of convalescent plasma among COVID-19 patients overall. Second, we did not have access to patient-level data for the studies included in this article. Thus, our subgroup analyses that separated patients by a single baseline characteristic were simplistic.165 Lack of patient-level data does not allow analyses using more complex statistical models that incorporate multiple characteristics,166 and previous studies have pooled patient-level data from clinical trials of COVID-19 convalescent plasma.6,49 Third, we limited our focus to a single outcome. Finally, we note that the preponderance of data in this analysis came from studies in the first years of the pandemic involving unvaccinated populations that were immunologically naïve to SARS-CoV-2, and today most individuals in the countries contributing the most studies are vaccinated and/or have previous experience with COVID-19, making the populations then and now immunologically different.

Conclusion

This systematic review and meta-analysis found that convalescent plasma was associated with a 13% decrease in mortality rates in hospitalized patients with COVID-19 compared with a control cohort. Subgroup analyses revealed that patients treated with high-titer plasma and patients treated earlier in the course of the disease benefited more from COVID-19 convalescent plasma transfusions. Thus, reasonable concerns about the use of low antibody-titer convalescent plasma later in the course of the disease remain. These findings can offer experts a new starting point in forming their judgment of the therapeutic effectiveness of COVID-19 convalescent plasma and may help transform subjective and nebulous insider views into a more transparent and reliable knowledge base. Finally, our findings support the deployment of convalescent plasma in future epidemic emergencies until better therapies are available, with the caveat that convalescent plasma should be administered early in disease using units with the highest antibody content available.

Potential Competing Interests

Drs Senefeld, Carter, Joyner, Fairweather, Bruno, and Wright reported being investigators in the US Expanded Access Program of COVID-19 convalescent plasma. Drs Paneth, Casadevall, and Joyner reported serving as leadership for the COVID-19 Convalescent Plasma Project outside the submitted work.

Acknowledgment

The authors requested to waive the reference limit for inclusion of all references included and data analyzed for this systematic review and meta-analysis. Dr Senefeld and Ms Gorman contributed equally as first authors to the work of the study and manuscript. Drs Casadevall and Joyner contributed equally as senior authors to the work of the study and manuscript.

Footnotes

Grant Support: This work was supported by the United Health Group, David and Lucile Packard Foundation, Schwab Charitable Fund (Eric E. Schmidt, Wendy Schmidt donors), National Basketball Association, and Mayo Clinic.

Supplemental material can be found online at http://www.mcpiqojournal.org. Supplemental material attached to journal articles has not been edited, and the authors take responsibility for the accuracy of all data.

Supplemental Online Material

Supplemental Data
mmc1.docx (992.1KB, docx)

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