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Impact of withholding breastfeeding around the time of Rotarix® vaccination
on the immunogenicity of Rotarix® vaccine
A Randomized Trial
S. Asad Ali, MD, MPHDepartment of Pediatrics and Child Health
Aga Khan UniversityPakistan
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Why is the immunogenicity of rotavirus vaccines lower in low income settings?
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Why is the immunogenicity of rotavirus vaccines lower in low income settings?
• Environmental Enteropathy
• Higher anti-RV antibodies in mother’s blood with transplacental transmission
• Higher anti-RV antibody levels in breast milk
• Concomitant OPV administration
• Coexistent intestinal infections3
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Why is the immunogenicity of rotavirus vaccines lower in low income settings?
• Environmental Enteropathy
• Higher anti-RV antibodies in mother’s blood with transplacental transmission
• Higher anti-RV antibody levels in breast milk
• Concomitant OPV administration
• Coexistent intestinal infections4
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FIGURE 1.
Cumulative frequency profiles of rotavirus-specific antibodies in breast milk specimens
from mothers in India, Vietnam, Korea and the United States. Milk specimens were tested
for IgA (A) and neutralizing activity against vaccine strains Rotarix (B), RotaTeq G1 (C),
and 116E (D) as described in the text. Nearly all Indian women had an IgA titier >16 versus
all other women. The median IgA and neutralizing titers and the distribution of titers for
breast milk from Indian women were higher than all others. The values of significance
between Indian women and those from Korea, Vietnam, and the United States are indicated.
NA indicates neutralizing antibody.
Moon et al. Page 8
Pediatr Infect Dis J . Author manuscript; available in PMC 2013 July 08.
NIH
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IH-P
A A
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A A
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Moon SS et al. Inhibitory effect of breast milk on infectivity of live oral rotavirus vaccines. Pediatr Infect Dis J. 2010
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Why is the immunogenicity of rotavirus vaccines lower in low income settings?
• Environmental Enteropathy
• Higher anti-RV antibodies in mother’s blood with transplacental transmission
• Higher anti-RV antibody levels in breast milk
• Concomitant OPV administration
• Coexistent intestinal infections6
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Primary Objective
To compare the immunogenicity of Rotarix® in infants
whose breastfeeding was withheld one hour before
through one hour after vaccination with each Rotarix®
dose to that in infants who were breastfed at the time of
vaccination
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Secondary Objective
To determine the effect of rotavirus neutralizing activity inbreast milk on the immunogenicity of Rotarix® vaccine ininfants
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Trialprofile
RV=RotarixVaccine
B=BloodDraw
Randomiza on
1:1
RV/B B
10weeks6weeks 14weeks 18weeks
(n=210)
(n=210)
RV RV/B
Birth
Breas eedingimmediatelybeforeRVadministra on
Breas eedingwithheldforonehourbeforeanda erRVadministra on
RV/B BRV RV/B
(n=200)
(n=200)
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Randomized (400)
Breastfeed Withholding group(200)
IgA≥20 U/mL (3)
Non-compliance with blood draw (1)
Lost to follow up/Dropout
Refusal (9)
Illness (1)
Moved from Study Area (5)
Per Protocol (181)
Immediate Breastfeeding group(200)
IgA≥20 U/mL (6)
Non-compliance with blood draw (1)
Non-compliance with breastfeeding schedule (5)
Lost to follow up/Dropout
Refusal (9)
Death (1)
Moved from Study Area (6)
Per Protocol (172)
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Withholding Arm(N = 200)
Immediate Breastfeed Arm(N = 200)
Male 45 % 54 %
Age in Weeks 6.3 (0.5) 6.3 (0.5)
Weight (g) at 6 weeks 3939.1 (619.2) 4047.5 (594.7)
Age of visit in weeks†
Visit 2 10.4 (0.5) 10.4 (0.6)Visit 3 14.6 (0.6) 14.6 (0.6)Visit 4 18.7 (0.7) 18.7 (0.7)
†per-protocol population
Baseline Characteristics and Age at visits
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Age at sample (weeks)
Withholding ArmImmediate
Breastfeed Arm
P-Value(N=181) (N=172)
Seroconversion
rate95 % CI
Seroconversion
rate95 % CI
14 (after 2 doses)
16.6% (11.8; 22.6) 29.1% (22.8; 36.2) 0.005
18 (after 3 doses)
28.2% (22.1; 35.1) 37.8% (30.8; 45.2) 0.070
Anti-rotavirus IgA antibody seroconversion rates in the per protocol population
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Age at sample (weeks)
Withholding ArmImmediate
Breastfeed Arm
P-Value(N=181) (N=172)
Seroconversion
rate95 % CI
Seroconversion
rate95 % CI
14 (after 2 doses)
16.6% (11.8; 22.6) 29.1% (22.8; 36.2) 0.005
18 (after 3 doses)
28.2% (22.1; 35.1) 37.8% (30.8; 45.2) 0.070
Anti-rotavirus IgA antibody seroconversion rates in the per protocol population
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Age at sample (weeks)
Withholding ArmImmediate
Breastfeed Arm
P-Value(N=181) (N=172)
Seroconversion
rate95 % CI
Seroconversion
rate95 % CI
14 (after 2 doses)
16.6% (11.8; 22.6) 29.1% (22.8; 36.2) 0.005
18 (after 3 doses)
28.2% (22.1; 35.1) 37.8% (30.8; 45.2) 0.070
Anti-rotavirus IgA antibody seroconversion rates in the per protocol population
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Anti-rotavirus IgA geometric mean titers (GMT) for seroconverted subjects after 2 or 3 doses
Age at Sample(weeks)
Withholding Arm Immediate Breastfeed Arm
n GMT 95 % CI n GMT 95 % CI P value
14 (after 2 doses)a 30 194.4 (126.2;299.3) 50 104.4 (77.3; 140.9) 0.016
18 (after 3 doses) b 51 125.4 (91.0; 172.9) 65 91.8 (69.1; 121.8) 0.147
aIncludes only anti-rotavirus IgA seropositive subjects at 14 weeksbIncludes only anti-rotavirus IgA seropositive subjects at 18 weeks
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Anti-rotavirus IgA geometric mean titers (GMT) for seroconverted subjects after 2 or 3 doses
Age at Sample(weeks)
Withholding Arm Immediate Breastfeed Arm
n GMT 95 % CI n GMT 95 % CI P value
14 (after 2 doses)a 30 194.4 (126.2;299.3) 50 104.4 (77.3; 140.9) 0.016
18 (after 3 doses) b 51 125.4 (91.0; 172.9) 65 91.8 (69.1; 121.8) 0.147
aIncludes only anti-rotavirus IgA seropositive subjects at 14 weeksbIncludes only anti-rotavirus IgA seropositive subjects at 18 weeks
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Anti-rotavirus IgA geometric mean titers (GMT) for seroconverted subjects after 2 or 3 doses
Age at Sample(weeks)
Withholding Arm Immediate Breastfeed Arm
n GMT 95 % CI n GMT 95 % CI P value
14 (after 2 doses)a 30 194.4 (126.2;299.3) 50 104.4 (77.3; 140.9) 0.016
18 (after 3 doses) b 51 125.4 (91.0; 172.9) 65 91.8 (69.1; 121.8) 0.147
aIncludes only anti-rotavirus IgA seropositive subjects at 14 weeksbIncludes only anti-rotavirus IgA seropositive subjects at 18 weeks
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Association of Maternally Derived Neutralizing Antibody (MDNA)* titers at 6 weeks with rotavirus seroconversion at
14 weeks (post 2 doses)
MDNA at 6 weeks(Percentile)
Withholding Arm Immediate Breastfeed Arm Combined
(N= 93) (N= 85) (N= 169)
Seroconversion rate Seroconversion rate Seroconversion rate
< 25 22.5% 38.8% 31.4%
> 75 5.7% 22.2% 12.4%
P= 0.026 P= 0.157 P =0.003
*MDNA measured using 89:12 strain, which is precursor to Rotarix vaccine
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Association of Maternally Derived Neutralizing Antibody (MDNA)* titers at 6 weeks with rotavirus seroconversion at
14 weeks (post 2 doses)
MDNA at 6 weeks(Percentile)
Withholding Arm Immediate Breastfeed Arm Combined
(N= 93) (N= 85) (N= 169)
Seroconversion rate Seroconversion rate Seroconversion rate
< 25 22.5% 38.8% 31.4%
> 75 5.7% 22.2% 12.4%
P= 0.026 P= 0.157 P =0.003
*MDNA measured using 89:12 strain, which is precursor to Rotarix vaccine
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Association of Maternally Derived Neutralizing Antibody (MDNA)* titers at 6 weeks with rotavirus seroconversion at
14 weeks (post 2 doses)
MDNA at 6 weeks(Percentile)
Withholding Arm Immediate Breastfeed Arm Combined
(N= 93) (N= 85) (N= 169)
Seroconversion rate Seroconversion rate Seroconversion rate
< 25 22.5% 38.8% 31.4%
> 75 5.7% 22.2% 12.4%
P= 0.026 P= 0.157 P =0.003
*MDNA measured using 89:12 strain, which is precursor to Rotarix vaccine
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Association of Maternally Derived Neutralizing Antibody (MDNA)* titers at 6 weeks with rotavirus seroconversion at
14 or 18 weeks (post 3 doses)
MDNA at 6 weeks(Percentile)
Withholding Arm Immediate Breastfeed Arm Combined
(N= 93) (N= 85) (N= 169)
Seroconversion rate Seroconversion rate Seroconversion rate
< 25 37.5% 46.9% 42.7%
> 75 11.3% 19.5% 14.6%
P= 0.005 P= 0.012 P <0.0001
*MDNA measured using 89:12 strain, which is precursor to Rotarix vaccine
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Association of Maternally Derived Neutralizing Antibody (MDNA)* titers at 6 weeks with rotavirus seroconversion at
14 or 18 weeks (post 3 doses)
MDNA at 6 weeks(Percentile)
Withholding Arm Immediate Breastfeed Arm Combined
(N= 93) (N= 85) (N= 169)
Seroconversion rate Seroconversion rate Seroconversion rate
< 25 37.5% 46.9% 42.7%
> 75 11.3% 19.5% 14.6%
P= 0.005 P= 0.012 P <0.0001
*MDNA measured using 89:12 strain, which is precursor to Rotarix vaccine
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Association of Maternally Derived Neutralizing Antibody (MDNA)* titers at 6 weeks with rotavirus seroconversion at
14 or 18 weeks (post 3 doses)
MDNA at 6 weeks(Percentile)
Withholding Arm Immediate Breastfeed Arm Combined
(N= 93) (N= 85) (N= 169)
Seroconversion rate Seroconversion rate Seroconversion rate
< 25 37.5% 46.9% 42.7%
> 75 11.3% 19.5% 14.6%
P= 0.005 P= 0.012 P <0.0001
*MDNA measured using 89:12 strain, which is precursor to Rotarix vaccine
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Low BMNA in Breast
Milk at 10 weeks
High BMNA in Breast
Milk at 10 weeks
Difference in
seroconversion P-value
(<50 %ile) (>50 %ile)
Time pointMDNA at 6
weeks Seroconversion rate Seroconversion rate
14 weeks (post 2
doses)
<50 %ile 44.4% 20% 24.4% 0.019
>50 %ile 29% 27.3% 1.8% 1
18 weeks (post 3
doses)
<50 %ile 38.9% 38% 0.9% 1
>50 %ile 45.2% 32.7% 12.4% 0.353
Serum Anti-Rotavirus IgA Seroconversion in Immediate Breastfeeding Group, by MDNA and 10-Week BMNA Level
MDNA Maternally derived neutralizing antibodies; BMNA Breast milk neutralizing activity
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Low BMNA in Breast
Milk at 10 weeks
High BMNA in Breast
Milk at 10 weeks
Difference in
seroconversion P-value
(<50 %ile) (>50 %ile)
Time pointMDNA at 6
weeks Seroconversion rate Seroconversion rate
14 weeks (post 2
doses)
<50 %ile 44.4% 20% 24.4% 0.019
>50 %ile 29% 27.3% 1.8% 1
18 weeks (post 3
doses)
<50 %ile 38.9% 38% 0.9% 1
>50 %ile 45.2% 32.7% 12.4% 0.353
Serum Anti-Rotavirus IgA Seroconversion in Immediate Breastfeeding Group, by MDNA and 10-Week BMNA Level
MDNA Maternally derived neutralizing antibodies; BMNA Breast milk neutralizing activity
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Low BMNA in Breast
Milk at 10 weeks
High BMNA in Breast
Milk at 10 weeks
Difference in
seroconversion P-value
(<50 %ile) (>50 %ile)
Time pointMDNA at 6
weeks Seroconversion rate Seroconversion rate
14 weeks (post 2
doses)
<50 %ile 44.4% 20% 24.4% 0.019
>50 %ile 29% 27.3% 1.8% 1
18 weeks (post 3
doses)
<50 %ile 38.9% 38% 0.9% 1
>50 %ile 45.2% 32.7% 12.4% 0.353
Serum Anti-Rotavirus IgA Seroconversion in Immediate Breastfeeding Group, by MDNA and 10-Week BMNA Level
MDNA Maternally derived neutralizing antibodies; BMNA Breast milk neutralizing activity
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Summary of Findings
• Withholding breast feeding around the time of RV1 vaccine administration did not lead to increased anti-rotavirus IgA seroconversion.
• To our surprise, IgA seroconversion after two RV1 doses at 6 and 10 weeks was significantly greater in immediately breastfed infants compared with those in whom breast milk was withheld!
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Some nuances!
• GMT in seropositive infants at 14 weeks was higher in the withholding arm compared to the immediate arm
• Lower seroconversion in infants in the immediate feeding arm with low MDNA/higher BMNA after two doses suggests that ingesting breast milk with higher BMNA at the same time as vaccine may reduce the immune response in some infants
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Summary
• Although serum rotavirus IgA is not a perfect correlate of protection, our findings suggest that substantially improved clinical protection is not likely with the strategy of withholding breastfeed around the time of vaccination.
• We suggest breastfeeding can continue ad lib around the time of RV1 administration.
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But why was serum rotavirus IgA seroconversionhigher in the immediate breastfeed group?
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• Chance finding?
• Additional buffering of gastric acid at the time of vaccine administration?
• Something immunogenic in breast milk ??
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Study Team:• Aga Khan University
Asad Ali (PI)
Momin Kazi
Anita Zaidi
Rota study team
Patients and their families
Margaret Cortese
Umesh Parashar
Baoming Jia
SungSil Moon
Jessica Fleming
Chris Victor
Kathy Neuzil
Duncan Steele
CDC
Monica McNeal
University of Cincinnati
PATH