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Grading of Recommendations, Assessment, Development, and Evaluation (GRADE): Moderna COVID-19 Vaccine for Persons Aged 12-17 Years										Related Pages
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			OverviewIntroductionMethodsResultsGRADE Summary
Overview
A Grading of Recommendations, Assessment, Development and Evaluation (GRADE) review of the evidence for benefits and harms for Moderna coronavirus disease 2019 (COVID-19) vaccine for persons aged 12-17 years was presented to the Advisory Committee for Immunization Practices (ACIP) on June 23, 2022. GRADE evidence type indicates the certainty in estimates from the available body of evidence. Evidence certainty ranges from type 1 (high certainty) to type 4 (very low certainty) [*1*].
The policy question was, “Should vaccination with Moderna COVID-19 vaccine (2 doses, 100 μg) be recommended for persons 12-17 years of age during an Emergency Use Authorization?” The potential benefits pre-specified by the ACIP COVID-19 Vaccines Work Group included prevention of symptomatic laboratory-confirmed COVID-19 (critical), hospitalization due to COVID-19 (important), multisystem inflammatory syndrome in children (MIS-C) (important), and asymptomatic SARS-CoV-2 infection (important). The two pre-specified harms were serious adverse events (SAEs) (critical) and reactogenicity grade ≥3 (important).
A systematic review of evidence on the efficacy and safety of a two-dose regimen of Moderna COVID-19 vaccine among persons aged 12-17 years was conducted. The quality of evidence from one Phase II/III randomized controlled trial was assessed using a modified GRADE approach.
A lower risk of symptomatic COVID-19 was observed among the vaccine group compared with the placebo group (Relative risk [RR]: 0.11; 95% Confidence Interval [CI]: 0.02, 0.50; evidence type 2). Immunobridging data were also assessed in support of efficacy. Among adolescents ages 12 – 17 years, the immune response to vaccine was non-inferior to that observed in adults ages 18-25 years ( GMR: 1.1; 95% CI: 0.9, 1.2; evidence type 2).  Additionally, a lower risk of asymptomatic SARS-CoV-2 infection was observed among the vaccine group compared with the placebo group, though the confidence interval was wide and crossed the null (RR: 0.61 (0.24, 1.54); evidence type 3). The available data indicated that SAEs were more common in vaccine recipients, but certainty in the estimate was very low (RR 1.50; 95% CI: 0.30, 7.40; evidence type 4), and none of these SAEs were assessed by the Food and Drug Administration (FDA) as related to study intervention. Reactogenicity grade ≥3 was associated with vaccination (RR 5.23; 95% CI: 4.05, 6.76; evidence type 1). About 25% of vaccine recipients and 5% of placebo recipients reported any grade ≥3 local or systemic reactions following either dose 1 or dose 2.
Introduction
On June 23, 2022, the FDA updated the Emergency Use Authorization (EUA) for Moderna (mRNA-1273) vaccine for prevention of symptomatic COVID-19 to include adolescents aged 12─17 years [*2*]. As part of the process employed by the ACIP, a systematic review and GRADE evaluation of the evidence for Moderna COVID-19 vaccine was conducted and presented to ACIP. The ACIP adopted a modified GRADE approach in 2010 as the framework for evaluating the scientific evidence that informs recommendations for vaccine use. Evidence of benefits and harms were reviewed based on the GRADE approach [*1*].
The policy question was, “Should vaccination with Moderna COVID-19 vaccine (2 doses, 100 μg) be recommended for persons 12-17 years of age during an Emergency Use Authorization?” (Table 1).
Methods
We conducted a systematic review of evidence on the efficacy and safety of a two-dose regimen (100 μg per dose) of Moderna COVID-19 vaccine. We assessed outcomes and evaluated the quality of evidence using the GRADE approach.
During Work Group calls, members were asked to pre-specify and rate the importance of relevant patient-important outcomes (including benefits and harms) before the GRADE assessment. No conflicts of interest were reported by CDC and ACIP COVID-19 Vaccines Work Group members involved in the GRADE analysis. Outcomes of interest included individual benefits and harms (Table 2). The critical benefit of interest was prevention of symptomatic laboratory-confirmed COVID-19. Other important outcomes included prevention of hospitalization due to COVID-19, prevention of MIS-C, and prevention of asymptomatic SARS-CoV-2 infection. The critical harm of interest was serious adverse events, including death; reactogenicity grade ≥3 was deemed an important harm. Hospitalization and prevention of MIS-C were not included in the evidence profile because no data were available.
We identified clinical trials through clinicaltrials.gov. Records of relevant Phase I, II, or III randomized controlled trials (RTCs) of COVID-19 vaccine were included if they 1) provided data on adolescents aged 12─17 years vaccinated with mRNA-1273; 2) involved human subjects; 3) reported primary data; and 4) included data relevant to the efficacy and safety outcomes being measured. We identified relevant observational studies through an ongoing systematic review conducted by the International Vaccine Access Center (IVAC) and the World Health Organization (WHO) [4]. Articles were included if they provided data on vaccination with the Moderna COVID-19 vaccine and 1) involved human subjects; 2) reported primary data; 3) included adolescents (ages 12-17) at risk for SARS-CoV-2 infection; 4) included data relevant to the efficacy and safety outcomes being measured; and 5) included data for the specific vaccine formulation, dosage, and timing being recommended (mRNA-1273, 100 μg, 0.5 mL 2 doses IM, 28 days apart). In addition, efforts were made to obtain unpublished and other relevant data by hand-searching reference lists, and consulting with vaccine manufacturers and subject matter experts. Titles and abstracts were screened independently and in duplicate by two separate reviewers. Characteristics of the included studies are shown in Appendix 1.
Patient-important outcomes (including benefits and harms) for assessment were selected by the Work Group during Work Group calls and via online surveys where members were asked to rate and rank the importance of relevant outcomes. The GRADE assessment across the body of evidence for each outcome was presented in an evidence profile.
Relative risks (RR) were calculated from numerators and denominators available in the body of evidence. Vaccine efficacy estimates were defined as 100% x (1-RR). In addition to data on symptomatic COVID-19 cases, immunobridging data comparing geometric mean neutralizing antibody titers (GMTs) in 12-17-year-olds to those in 18-25-year-olds in whom clinical efficacy was previously established was provided using a geometric mean ratio (GMR).
The evidence certainty assessment addressed risk of bias, inconsistency, indirectness, imprecision, and other characteristics. The GRADE assessment across the body of evidence for each outcome was presented in an evidence profile; the evidence certainty of Type 1, 2, 3, or 4 corresponds to high, moderate, low, or very low certainty, respectively.
Results
The results of the GRADE assessment were presented to ACIP on June 23, 2022. One study was reviewed that provided data on outcomes specified for GRADE (Appendix 1). Data were reviewed from one Phase II/III randomized controlled trial using data provided by the sponsor [*3*]. Symptomatic laboratory confirmed COVID-19 occurred less frequently in the Moderna COVID-19 vaccination group when compared to the placebo group (vaccine efficacy [VE]: 89.2%; 95% CI: 49.9–97.6%; based on RR: 0.11; 95% CI: 0.02, 0.50) (Table 3a, Table 4). Serious concern for imprecision was noted due to the small number of events and potential for fragility in the estimate. We also note that the RCT excluded persons with a history of COVID-19, pregnant or breastfeeding women, immunocompromised persons and persons who have medical or psychiatric condition that, according to the investigator’s judgment, may pose additional risk as a result of participation, interfere with safety assessments, or interfere with interpretation of results. Due to these exclusions, the clinical trial participants may not represent all persons aged 12-17 years.  The immune response to the Moderna COVID-19 vaccine among adolescents aged 12-17 years was non-inferior (GMR: 1.1; 95% CI: 0.9, 1.2) to the immune response among adults aged 18-25 years receiving the Moderna COVID-19 vaccine in whom clinical efficacy had been established (Table 3b).  Serious concern of indirectness was noted because immunobridging is a surrogate measure of efficacy. Asymptomatic SARS-CoV-2 infection occurred less frequently in the vaccination group when compared to the placebo group (vaccine efficacy: 36.1%; 95% CI: -22.0–66.5%; based on RR: 0.64; 95% CI: 0.34, 1.22) (Table 3c, Table 4). Very serious concerns of imprecision were noted due to the confidence interval containing estimates for which different policy decisions would be made and failure to meet minimum information requirements.
For evaluation of potential harms, data were reviewed from the Phase II/III randomized controlled trial. Serious adverse events were more common in vaccine recipients, but certainty in the estimate was very low (RR: 1.50; 95% CI: 0.30, 7.40). There was serious concern of indirectness because the body of evidence does not provide certainty that rare serious adverse events were captured due to the short follow-up (median 2-months) and exclusion criteria, listed previously. Very serious concerns of imprecision were noted due to the confidence interval containing estimates for which different policy decisions would be made and failure to meet minimum information requirements. No SAEs were judged by FDA to be related to vaccination (Table 3d). There were no cases of vaccine-associated enhanced disease or deaths. Grade ≥3, or severe, local or systemic reactions within 7 days following either vaccination, were reported by 25.3% of vaccine recipients, and occurred more frequently in the vaccine than placebo group (Table 3e). No serious concerns impacted the certainty of the estimate of reactogenicity.
GRADE Summary
The initial GRADE evidence level was type 1 (high) for each outcome because the body of evidence was from randomized controlled trials (Table 4). In terms of benefits, the available data indicated that the vaccine was efficacious for preventing symptomatic COVID-19, and the certainty was downgraded once for imprecision due to the small number of events (type 2, moderate). Efficacy assessed with immunobridging was downgraded once for indirectness because it was a surrogate outcome (type 2, moderate). The outcome of prevention of asymptomatic SARS-CoV-2 infection was downgraded twice for very serious concerns of imprecision due to the confidence interval containing estimates for which different policy decisions would be made and failure to meet minimum information requirements. The certainty in the estimate of the effect for serious adverse events was downgraded one point due to serious concern of indirectness related to the short duration of follow up (median two months) and twice for very serious concerns of imprecision due to the confidence interval containing estimates for which different policy decisions would be made and failure to meet minimum information requirements (type 4, very low certainty). No serious concerns impacted the certainty in the estimate of reactogenicity (type 1, high) (Table 4).
References
Ahmed F. U.S. Advisory Committee on Immunization Practices (ACIP) Handbook for Developing Evidence-based Recommendations[53 pages].
Food and Drug Administration. Moderna COVID-19 Vaccine Emergency Use Authorization. Moderna COVID-19 Vaccine EUA Letter of Authorization 03292022 (fda.gov). Accessed June 21, 2022.
Moderna, 2021 personal communication, June 2021-May 2022.
International Vaccine Access Center (IVAC), Johns Hopkins Bloomberg School of Public Health. VIEW-hub. www.view-hub.org. Accessed: 4/29/2022.Table 1: Policy Question and PICO
Table 1: Policy Question and PICO
Policy question:
Should vaccination with Moderna COVID-19 vaccine (2-doses, IM) be recommended for adolescents aged 12-17 years?Population
Persons aged 12-17 yearsIntervention
Moderna COVID-19 vaccine mRNA-1273 (100 μg, 2 doses IM, 28 days apart)Comparison
No Moderna COVID-19 vaccineOutcomes
Symptomatic laboratory-confirmed COVID-19
Hospitalization due to COVID-19
Multisystem inflammatory syndrome in children (MIS-C)
Asymptomatic SARS-CoV-2 infection
Serious adverse events
Reactogenicity grade ≥3**Abbreviations**: IM = intramuscular.
Table 2: Outcomes and Rankings
Table 2: Outcomes and Rankings
Outcome
Importance
Included in evidence profileSymptomatic laboratory-confirmed COVID-19
Critical
YesHospitalization due to COVID-19
Important
NoaMultisystem inflammatory syndrome in children (MIS-C)
Important
NoaAsymptomatic SARS-CoV-2 infection
Important
YesSerious adverse events
Critical
YesReactogenicity grade ≥3
Important
Yes
aNo events were observed in study identified in the review of evidence.
Table 3a: Summary of Studies Reporting Symptomatic Laboratory-confirmed COVID-19
Table 3a: Summary of Studies Reporting Symptomatic COVID-19 (PCR-confirmed)
Authors last name, pub year
Age or other characteristic of importance
n/**N (%)** intervention
n/**N (%)** comparison
Comparator
Vaccine Efficacy (95% CI) [100 x (1-RR)]
Study limitations (Risk of Bias)Moderna, 2021 [3]a
SARS-CoV-2 RT-PCR-positive symptomatic illnessb, in seronegativec persons aged 12-17 years, ≥14 days post second dose
2/2142 (<0.1%)
9/1045 (0.9%)
Placebo
89.2% (49.9%, 97.6%)
Not serious**Abbreviations:** RT-PCR = real-time polymerase chain reaction; CI = confidence interval; RR = relative risk.
aBased on data cutoff May 31, 2021; participants had a median of almost 2 months of follow-up.
bRT-PCR symptomatic illness defined as: a positive post-baseline PCR result and one or more of the following systemic symptoms: fever (temperature ≥38oC), or chills, cough, shortness of breath or difficulty breathing, fatigue, muscle aches, or body aches, headache, new loss of taste or smell, sore throat, nasal congestion or rhinorrhea, nausea, or vomiting or diarrhea
cNegative status at baseline was defined as a negative RT-PCR test for SARS-CoV-2 and a negative serology test based on bAb specific to SARS-CoV-2 nucleocapsid on or before Day 1.
Table 3b: Summary of Studies Reporting Symptomatic Laboratory-confirmed COVID-19 (assessed using immunobridging)
Table 3b: Summary of Studies Reporting Symptomatic Laboratory-confirmed COVID-19 (assessed using immunobridging)
Authors last name, pub year
Age or other characteristic of importance
n
12-17 Years
n
18-25 Years
GMRc
(95%CI)
Met Noninferiority Objectived
Study limitations (Risk of Bias)Moderna, 2021 [*3*]a
Serum antibody level by pseudovirus neutralization (ID50)b
340
296
1.08 (0.9, 1.2)
Yes
Not serious**Abbreviations:** ID50 = 50% inhibitory dose; GMR= geometric mean ratio; CI = confidence interval
aImmune response was measured at Day 57
bAmong participants immunologic or virologic evidence of prior COVID-19 (i.e., negative NP swab test at Day 1 and/or binding antibodies against SARS-CoV-2 nucleocapsid below limit of detection or lower limit of quantification) at Day 1 before the first dose of IP.
cGMRs and 2-sided 95% CIs were calculated by exponentiating the mean difference of the logarithms of the titers (Group 1 [12-17 years] – Group 2 [18-25 years]) and the corresponding CI (based on the Student t distribution).
dNoninferiority is declared if the lower bound of the 2-sided 95% CI for the GMR is greater than 0.67.
Table 3c: Summary of Studies Reporting Asymptomatic SARS-CoV-2 Infection
Table 3c: Summary of Studies Reporting Serious Adverse Events
Authors last name, pub year
Age or other characteristic of importance
n/N (%) intervention
n/N (%) comparison
Comparator
**Vaccine Efficacy (95% CI) [100 x (1-RR)]**
Study limitations (Risk of Bias)Moderna, 2021 [*3*]
Asymptomatic SARS-CoV-2a
21/2162 (1.0%)
16/1073 (1.5%)
Placebo
34.9% (-24.3%, 65.9%)
Not serious**Abbreviations:**RT-PCR = real-time polymerase chain reaction; CI = confidence interval; RR = relative risk
aAbsence of symptoms AND bAb levels against SARS-CoV-2 nucleocapsid protein negative at Day 1 then becomes positive starting at day 57 OR positive RT-PCR counted 14 days after the second dose with negative SARS-CoV-2 at baseline
Table 3d: Summary of Studies Reporting Serious Adverse Events
Table 3d: Summary of Studies Reporting Serious Adverse Events
Authors last name, pub year
Age or other characteristic of importance
**nb/Nc (%) intervention**
**nb/Nc (%) comparison**
Comparator
RR (95% CI)
Study limitations (Risk of Bias)Moderna, 2021 [*3*]
Persons aged 12-17 years
6/2486 (0.2%)b
2/1240 (0.2%)b
Placebo
1.50 (0.30, 7.40)
Not serious
**Abbreviations:**RR = relative risk; CI = confidence interval; RCT = randomized controlled trial.
aDeath, life-threatening event, hospitalization, incapacity to perform normal life functions, medically important event, or congenital anomaly/birth defect
bNumber of participants experiencing SAEs (participants may experience more than one SAE)
cIncluded all randomized participants who received at least 1 dose of vaccine.
Table 3e: Summary of Studies Reporting Reactogenicity
Table 3e: Summary of Studies Reporting Reactogenicity
Authors last name, pub year
Age or other characteristic of importance
**n/N (%) intervention**
**n/N (%) comparison**
Comparator
RR (95% CI)
Study limitations (Risk of Bias)Moderna, 2021 [3]b
Persons aged 12-17 years
629/2485 (25.3%)
60/1240 (4.8%)
Placebo
5.2 (4.1, 6.8)
Not serious
**Abbreviations:**RR = relative risk; CI = confidence interval; RCT = randomized controlled trial.
aReactogenicity outcome includes local and systemic events, grade ≥3. Grade 3: prevents daily routine activity or requires use of a pain reliever. Grade 4: requires emergency room visit or hospitalization. One participant in the vaccine group reported grade 4 pyrexia (40.4 °C).
bBased on interim analysis, data cutoff May 8, 2021.
Table 4. Grade Summary of Findings Table
Table 4. Grade Summary of Findings Table
Certainty assessment
No of patients
Effect
Certainty
ImportanceNo of studies
Study design
Risk of bias
Inconsistency
Indirectness
Imprecision
Other considerations
Moderna COVID-19 vaccine, 100 mcg, 2 doses 28 days apart
No vaccine
Relative (95% CI)
Absolute (95% CI)Symptomatic laboratory-confirmed COVID-191
RCT
not seriousa
not serious
not seriousb,c,d
seriouse
none
2/2142 (0.1%)
9/1045 (0.9%)
**RR 0.11**
(0.02 to 0.50)
**767 fewer per 100,000**
(from 844 fewer to 431 fewer)
**Type 2**
Moderate
CRITICALSymptomatic laboratory-confirmed COVID-19 (assessed with immunobridging)1
RCT
not serious
not serious
seriousf,g
not serious
none
–
–
h
i
**Type 2**
Moderate
CRITICALAsymptomatic SARS-CoV-2 infection1
RCT
not serious
not serious
seriousd
very seriousj
none
21/2139 (1.0%)
16/1042 (1.5%)
**RR 0.64**
(0.34 to 1.22)
**553****fewer per 100,000**
(from 1,013 fewer to 338 more)
**Type 3**
Low
IMPORTANTSerious adverse events1
RCT
not seriousk
not serious
seriousd,l
very seriousi
none
6/2486 (0.2%)
2/1240 (0.2%)
**RR 1.5**
(0.3 to 7.4)
**100 more per 100,000**
(from 100 fewer to 1,000 more)
**Type 4**
Very Low
CRITICALReactogenicity, grade ≥31
RCT
not serious
not serious
not seriousd
not serious
none
629/2485 (25.3%)
60/1240 (4.8%)
**RR 5.2**
(4.1 to 6.8)
**20,323 more per 100,000**
(from 15,000 more to 28,065 more)
**Type 1**
High
IMPORTANT
**Abbreviations:**CI = confidence interval; RR = relative risk; COVID-19 = coronavirus disease 2019; RCT = randomized controlled trial.
Risk of bias related to blinding of participants and personnel was present. Although participants and study staff were blinded to intervention assignments, they may have inferred receipt of vaccine or placebo based on reactogenicity. This was deemed unlikely to overestimate efficacy, therefore the risk of bias was rated as not serious.
The effects noted are from an analysis of the evaluable efficacy population with outcomes assessed at least 14 days post dose 2 among persons who received two doses and had no evidence of prior SARS-CoV-2 infection.
An additional surrogate outcome of efficacy (immunogenicity) was identified. The immune response in 12–17-year-olds was non-inferior to adults 18-25 years, and consistent with efficacy results.
The RCT excluded persons with prior COVID-19 diagnosis, pregnant or breastfeeding women, persons who were immunocompromised, and persons who have a medical or psychiatric condition that, according to the investigator’s judgment, may pose additional risk as a result of participation, interfere with safety assessments, or interfere with interpretation of results. The population included in the RCT may not represent all persons aged 12-17 years.
Serious concern for imprecision was noted due to the small number of events and potential for fragility in the estimate.
Indirectness noted because immunogenicity is an indirect measure of efficacy.
The RCT excluded persons with prior COVID-19 diagnosis, pregnant or breastfeeding women, and persons who were immunocompromised. The population included in the RCT may not represent all persons aged 12-17 years.
The immune response to vaccine was evaluated using the geometric mean titer ratio of adolescents to young adults. Non-inferiority criteria are met when the lower bound of the 95% confidence interval for the ratio comparing the geometric mean neutralizing antibody titer for the two groups is not less than a pre-set value, which for this study was 0.67. The immune response to vaccine in adolescents aged 12-17 (GMT: 1401.7 [1276.3, 1539.4]) years was non-inferior to that observed in young adults aged 18-25 years (GMT: 1301.3 [1177.0, 1439.0]), with a geometric mean ratio of 1.1 (0.9-1.2), based on SARS-CoV-2 neutralization titers at 1 month after dose 2, in participants without prior evidence of SARS-CoV-2 infection.
Absolute effect not applicable for immunobridging outcome.
Very serious concern for imprecision was noted based on the confidence interval containing estimates for which different policy decisions would be made and failure to meet minimum information requirements.
Risk of bias related to blinding of participants was present. Although participants and study staff were blinded to intervention assignments, they may have inferred receipt of vaccine or placebo based on reactogenicity. Some reactogenicity outcomes may also have been reported as serious adverse events, and experiences of reactions immediately after vaccination could have influenced recall or reporting of subsequent serious adverse events. This was rated as not serious.
Serious concern of indirectness was noted. The body of evidence does not provide certainty that rare serious adverse events were captured due to the median 2-month follow-up and the sample size.Appendix 1. Studies Included in the Review of Evidence
Appendix 1. Studies Included in the Review of Evidence
Last name first author, Publication year
Study design
Country (or more detail, if needed)
**Population**
Total population
N Intervention
N comparison
Outcomes
Funding sourceModerna, 2021 [*3*]
Phase II/III RCT
USA
Persons aged 12-17 years
3725
2486
1240
Symptomatic laboratory-confirmed COVID-19
Asymptomatic SARS-CoV-2 infection
Serious adverse events
Reactogenicity
Industry funded**Abbreviations:** RCT = randomized controlled trial; COVID-19 = coronavirus disease 2019.
Appendix 2. Databases and strategies used for systematic review
Appendix 2. Databases and strategies used for systematic review
Database
Strategy**Clinicaltrails.gov**
**Inclusion:** Relevant Phase 1, 2, or 3 randomized controlled trials of COVID-19 vaccine
Search criteria:
Condition or disease: “COVID-19”
Other terms: “mRNA-1273” “Moderna”
Age group (advance search): Child (birth-17)
Phase (advanced search): Phase 1, Phase 2, Phase 3**Additional resources:** Unpublished and other relevant data by consulting with vaccine manufacturers and subject matter experts**International Vaccine Access Center (IVAC)**
**Inclusion criteria for IVAC systematic review:**
Published or preprint study with adequate scientific details
Includes groups with and without infection or disease outcome
Laboratory confirmed outcome
Vaccination status confirmed in ≥90%
Studies assess one vaccine or pooled mRNA vaccines
Includes participants who did or did not receive a COVID-19 vaccineVaccine effectiveness estimate calculated comparing vaccinated to unvaccinated**
**Additional criteria for GRADE review:**
Restricted to PICO-defined population, intervention, comparison, and outcomes
Outcomes assessed 7 to 14 days after 2nd dose
Only Moderna vaccine (not mRNA vaccines as a group)
Included studies of persons aged 12-17 yearsa. Most recent search conducted April 29, 2022.
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