Assessment of humoral immune response to two mRNA SARS-CoV-2 vaccines (Moderna and Pfizer) in healthcare workers fully vaccinated with and without a history of previous infection

J Appl Mic obiol. 2022;133:1969–1974.
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1969
wileyonlinelib a y.com/jou nal/jam
Recei ed: 8 Ap il 2022
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Re ised: 1 July 2022
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Accep ed: 5 July 2022
DOI: 10.1111/jam.15699
ORIGINAL ARTICLE
Assessmen o humo al immune esponse o wo mRNA
SARS- CoV- 2 accines (Mode na and P ize ) in heal hca e
wo ke s ully accina ed wi h and wi hou a his o y o
p e ious in ec ion
Lau aSe ano1,2
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SoniaAlga a e3,4
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Bea izHe e o- Co ina2,5,6
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JessicaBueno3
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Ma ía T.González- Ba iga1
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Ma íaDucons3
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JesicaMon e o- Ma co2,5
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Bea izAcha1,2
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AnaTaboada1,2
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Pila Sanz- Bu illo1,2
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C is inaYus e1,2
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Ra aelBeni o2,3,4
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on behal o he RIPOVAC S udy G oup
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s use, dis ibu ion and ep oduc ion in any medium, p o ided
he o iginal wo k is p ope ly ci ed.
© 2022 The Au ho s. Jou nal o Applied Mic obiology published by John Wiley & Sons L d on behal o Socie y o Applied Mic obiology.
Membe s o he RIPOVAC S udy G oup a e as ollows: L. Se ano, T. González, B. Acha, C. Yus e, P. Sanz, A. Taboada, C.I. Fe ández, P. Sahuquillo,
E. Zueco, J. Mon e o- Ma co and M. Cha lo (Hospi al Clínico Uni e si a io Lozano Blesa and IIS A agón), M. Redondo, L. Fe nández, C. Inglés and J.
Bueno (Hospi al Clínico Uni e si a io Lozano Blesa), R. Beni o (Hospi al Clínico Uni e si a io Lozano Blesa, Uni e sidad de Za agoza and IIS
A agón), S. Alga a e (Hospi al Clínico Uni e si a io Lozano Blesa and Uni e sidad de Za agoza), B. He e o- Co ina (Hospi al Clínico Uni e si a io
Lozano Blesa, IIS A agón and Uni e sidad San Jo ge).
1Occupa ional Heal h Uni , Lozano
Blesa Uni e si y Hospi al, Za agoza,
Spain
2Ins i u e o Heal h Resea ch A agón,
Za agoza, Spain
3Mic obiology Depa men , Lozano
Blesa Uni e si y Hospi al, Za agoza,
Spain
4Mic obiology Depa men , Za agoza
Uni e si y, Za agoza, Spain
5In es iga ion Uni , Lozano Blesa
Uni e si y Hospi al, Za agoza, Spain
6Uni e sidad San Jo ge, Villanue a de
Gállego, Za agoza, Spain
Co espondence
Ra ael Beni o, Lozano Blesa Uni e si y
Hospi al, Za agoza, Spain.
Email: beni o@uniza .es
Abs ac
Aims: P esence o an i- S1 egion o SARS- CoV- 2 spike p o ein was analysed, a wo
and eigh mon hs, in 477 immunocompe en heal hca e wo ke s in Za agoza, Spain,
accina ed wi h mRNA- 1273 (Mode na) o BNT162b2 (P ize ).
Me hods and esul s: An ibody analysis was pe o med wi h Alini y i Sys em
(Abbo ). A 2 mon hs, 100% o accina ed had an i- S1 IgG (mean=13,285 AU ml−1).
This alue was signi ican ly highe wi h Mode na (18,192 AU ml−1) han wi h P ize
(10,441 AU ml−1). The mean alue o an i- S1 IgG a e accina ion was signi ican ly
highe in pa ien s wi h han wi hou p e ious in ec ion (18,539 s. 7919 AU ml−1);
in bo h g oups was signi ican ly highe wi h Mode na han wi h P ize (21,881 s.
15,733 AU ml−1 and 11,949 s. 6387 AU ml−1), espec i ely. A 8 mon hs, 100% o pa ien s
we e IgG posi i e, wi h highe le els wi h Mode na han wi h P ize . Ne e heless, in
ensemble o cases, a mean dec ease o an ibody le els o 11,025 AU ml−1 was obse ed.
Conclusion: A 2 and 8 mon hs a e accina ion, IgG esponse pe sis s wi h bo h
accines bu wi h impo an dec ease which sugges s he need o e accina ion.
Signi icance and impac o s udy: The s udy con ibu es o know he immune s a-
us a e accina ion wi h wo o mo e used an i- SARS- CoV- 2 accines. This knowl-
edge is impo an o es ablishing he bes accina ion s a egy
KEYWORDS
an i- S IgG SARS- CoV- 2, heal hca e wo ke s, immune esponse, Mode na, mRNA SARS- CoV- 2
accines, P ize , pos - accina ion, RIPOVAC
Funding in o ma ion
This esea ch did no ecei e any
speci ic g an o unding agencies in
he public, comme cial o no - o -p o i
sec o s.
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1970
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SERRANO e al.
INTRODUCTION
The ecen ollou o accines ha induce speci ic an i-
bodies o SARS- CoV- 2 has p o ided an impo an ool in
con olling he pandemic.
The se ology o SARS- CoV- 2, in addi ion o being a
complemen a y ool in he diagnosis (Fuen es e al.,2021),
allows knowing he immune s a us o he pa ien a e
na u al in ec ion o a e accina ion (Okba e al.,2020).
SARS- CoV- 2 induces an ibody o ma ion agains S
(spike) and N (nucleocapsid) p o eins. An i- S1 IgG may
ha e neu alizing ac i i y. This ac i i y can be e alu-
a ed in i o wi h he pla e educ ion neu aliza ion
es , which is di icul o be applied o ou ine (San iago
e al.,2021). Fo his eason, diagnos ic es s ha e been
manu ac u ed o he quan i a i e measu emen o hese
an ibodies o es ablish he deg ee and du a ion o immu-
ni y and, based on hem, o de elop p e en i e accina-
ion s a egies.
We p esen da a om he obse a ional and p ospec-
i e RIPOVAC s udy in a g oup o heal hca e wo ke s in
A agón (Spain). This s udy aims o quan i y he esponse
o IgG agains he egion o he S1 subuni o he SARS-
CoV- 2 spike p o ein ha binds o he ecep o - binding
domain (RBD) (an i- S1 IgG) and o IgM agains he spike
p o ein (an i- S IgM), wo and 8 mon hs a e accina ion
wi h wo doses o wo i s - gene a ion mRNA accines,
Mode na (mRNA- 1273) o P ize - BioNTech (BNT162b2)
(wi h he in e al ime ecommended by he manu ac-
u e , 28 o 21 days, espec i ely), and he in luence on i
o p e- accina ion SARS- CoV- 2 in ec ion.
MATERIALS AND METHODS
We show da a om he RIPOVAC s udy, conduc ed a he
Lozano Blesa Uni e si y Clinical Hospi al o Za agoza,
Spain, he e e ence cen e o Sec o III o he A agón
Heal h Se ice (SALUD). Ini ially, 494 cases we e in-
cluded, belonging o all ca ego ies o heal hca e wo ke s,
bu 17 (3.44%) we e los . Finally, 477 olun a y, immu-
nocompe en , non- p egnan heal hca e wo ke s (71 male
and 406 emale, mean age o 45,29 yea s) accina ed wi h
Mode na o P ize , acco ding o he a ailabili y, be ween
Feb ua y and Ma ch 2021 we e included. Cases wi h
SARS- CoV- 2 in ec ion be ween he i s dose and he im-
munogenici y analysis we e excluded.
The i s pos - accine sample was ob ained om 477
heal hca e wo ke s [Mode na 175 (36.69%) and P ize 302
(63.31%)] 2 mon hs a e he second dose ±7 days (mon hs
o Ap il, May and June 2021), sho ly a e he peak o an-
ibodies was eached (Mon oya e al.,2021).
Table1 shows he dis ibu ion o 477 heal hca e wo k-
e s by sex, age, ype o accine and exis ence o no o
p e ious in ec ion. Women p edomina e in bo h g oups
accina ed wi h Mode na and P ize , bu wi hou signi -
ican di e ences in age.
Second sample was ob ained om 444 wo ke s, 53
male y 391 emale, wi h mean age o 45,61 yea s [Mode na
166 (37.39%) and P ize 278 (62.61%)] 8 mon hs a e he
second dose.
People wi h p e ious posi i e PCR o SARS- CoV- 2
(Alini y m, Abbo ; Viasu e, Ce es Bio ec; o GeneXpe ,
Cepheid), o wi h p e ious posi i e SARS- CoV- 2 an igen
(PanBio COVID- 19 Ag, Abbo ) o wi h p esence o an-
i- N IgG (SARS- CoV- 2 IgG, Abbo ) we e conside ed p e-
iously in ec ed.
The de e mina ion o quan i a i e an i- S1 IgG
(AU ml−1) and an i- S IgM (index) was pe o med by CMIA
(SARS- CoV- 2 IgG II Quan , Abbo and SARS- CoV- 2 IgM,
Abbo , espec i ely) by blinded, ained labo a o y s a ,
using he Abbo Alini y i pla o m, ollowing he manu-
ac u e 's ins uc ions. These eagen ki s ha e a speci ic-
i y o 100% and sensi i i y a 15 days o 98.77%, acco ding
o he manu ac u e .
The analysis was ca ied ou based on he accine e-
cei ed, Mode na (175 cases) o P ize (302 cases), and he
exis ence o no o a p e ious SARS- CoV- 2 in ec ion.
The p o ocol was app o ed by he Clinical In es iga ion
E hics Commi ee o A agón (EPA 21/000) and he e-
c ui ed heal hca e wo ke s ga e hei w i en in o med
TABLE 1 Cha ac e is ics o 477 en olled heal hca e wo ke s
Vaccine ype
Sex (%)
mean age
(SD)
P e ious in ec ion Yes No
Yes No
Mode na (175)
28 male
(16.00%)
42.14 (13.59)
22 (12.57%) 6 (3.43%)
147 emale
(84.00%)
43.31 (11.94)
88 (50.29%) 59 (33.71%)
P ize (302)
43 male
(14.24%)
Age: 45.71
(SD
12.36)
23 (7.62%) 20 (6.62%)
259 emale
(85.76%)
Age: 46.77
(SD
11.57)
108 (35.76%) 151 (50.00%)
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1971
RESPONSE TO TWO SARS- COV- 2 VACCINES
consen , ollowing he guidelines o he Decla a ion o
Helsinki.
S a is ical analysis
Quan i a i e a iables we e desc ibed using he mean
(s anda d de ia ion) and ca ego ical a iables we e e-
po ed using equencies. Di e ences in sociodemo-
g aphic and se ological da a be ween he g oups we e
es ed using he independen s uden 's - es o he Mann–
Whi ney U- es and epo ed as mean di e ence (95%
con idence in e al, CI). S a is ical signi icance was se a
p < 0.05 o all calcula ions. Da a analysis was pe o med
using SPSS .19 (IBM, Chicago, IL, USA).
RESULTS
All 477 ec ui ed heal hca e wo ke s we e an i- S1 IgG
posi i e a 2 mon hs a e accina ion, ega dless o he
ype o accine ecei ed. The esponses anged om 200
o >40,000 AU ml−1, wi h a mean o 13,285 AU ml−1 (95%
CI: 12,317 o 14,253) (Table2). Only 5 cases (1.05%) had
an i- S1 IgG alues <1000AU ml−1.
Ne e heless, an i- S IgM was only posi i e in 110 cases
(23.06%), wi h a mean index o 2.95 (SD 2.45, ange 1.00 o
14.93) (Table2). 50% o he an i- S IgM posi i e cases had
indexes be ween 1.00 and 2.00.
In Mode na- accina ed g oup (175 cases), he an i- S1
IgG mean was 18,192 AU ml−1 (95% CI 16,468 o 19,917),
signi ican ly highe han in he g oup accina ed wi h
P ize (10,441 AU ml−1, 95% CI 9406 o 11,477). Mean
di e ence be ween Mode na and P ize was 7751 (95% CI:
5866 o 9635) (p < 0.001). The same pe o mance was seen
o IgM, al hough wi hou signi ican di e ences, showing
a highe pe cen age o posi i i y and a highe mean index
o Mode na han o P ize , wi h pe cen ages o 23.43%
and 22.85%, and a e age indexes o 3.06 (95% CI: 2.18 o
3.83) and 2.89 (95% CI: 2.35 o 3.33), espec i ely (Table2).
In cases wi hou p e ious in ec ion, an i- S1 IgG e-
sponse was signi ican ly mo e in ense wi h Mode na
(11,949 AU ml−1, 95% CI, 9974 o 13,924) han wi h P ize
(6387 AU ml−1, 95% CI: 5579 o 7196). Mean di e ence
be ween Mode na and P ize was 5562 (95% CI: 3787 o
7336) (p < 0.001). An i- S1 IgM esponse was also g ea e
bo h in e ms o pe cen age and mean alues (Table3),
bu wi hou signi ican di e ences.
In cases wi h his o y o p e ious in ec ion, an i- S1 IgG
esponse wi h Mode na accine has been signi ican ly
mo e in ense, wi h a mean alue o 21,881 AU ml−1 (95% CI:
19,655 o 24,109) e sus 15,733 AU ml−1 wi h P ize (95%
CI: 13,951 o 17,515). Mean di e ence be ween Mode na y
P ize was 6149 (95% CI: 3344 o 8953) (p < 0.001) (Table4).
The esponse in cases wi h p e ious in ec ion is highe
han in pa ien s wi hou p e ious in ec ion.
In con as , he an i- S IgM esponse has been s on-
ge a e he P ize accine, bo h in pe cen age and mean
e ms, bu wi hou signi ican di e ences (Table4).
The 444 heal hca e wo ke s analysed 8 mon hs a e
he second dose also p esen an i- S, wi h a mean alue
o 4297 AU ml−1 wi h Mode na (SD 6289; ange 132–
>40,000) and o 3449 wi h P ize (SD 6645; ange 120–
>40,000) (Table5). An ibody le els wi h Mode na we e
signi ican ly highe han wi h P lze , also 8 mon hs a e
accina ion. (p< 0.001).
TABLE 2 IgG and IgM esponse in o al popula ion and accine ype
Vaccine Pa ien s
IgG ANTI- S1 IgM ANTI- S
Posi i e
Mean AU ml−1
(SD) Range Posi i e
Mean index
(SD) Range
Mode na 175 175 (100%) 18,192 (11556) 2111– >40,000 41 (23.43%) 3.06 (2.76) 1.03– 12.28
P ize 302 302 (100%) 10,441 (9144) 200– >40,000 69 (22.85%) 2.89 (2.27) 1.00– 14.93
To al 477 477 (100%) 13,285 (10755) 200– >40,000 110 (23.06%) 2.95 (2.45) 1.00– 14.93
TABLE 3 IgG and IgM esponse in o al popula ion and accine ype in non- in ec ed pa ien s
Vaccine Pa ien s
IgG an i- S1 IgM an i- S
Posi i e
Mean AU ml−1
(SD) Range Posi i e
Mean index
(SD) Range
Mode na 65 65 (100%) 11,949 (7971) 2111– >40,000 8 (12.30%) 4.83 (4.23) 1.32– 12.28
P ize 171 171 (100%) 6387 (5355) 715– 36,122 19 (11.11%) 2.63 (1.95) 1.20– 7.73
To al 236 236 (100%) 7919 (6651) 715– >40,000 27 (11.44%) 3.28 (2.91) 1.20– 12.28
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1972
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SERRANO e al.
O he 444 heal h wo ke s who we e analysed a eigh
mon hs, an ibody le els had diminished in 416 (93.69%)
and inc eased in 25 (5.63%). A leas ou o he la e had
been in ec ed a e he i s ex ac ion (PCR o posi i e
an i- N IgG). In he emaining 3 (0.68%), no change could
be demons a ed, because bo h samples p esen ed an an i-
body le el > 40,000 AU ml−1 (Table6).
A 8 mon hs, an ibody le el dec eased by a mean o
11,025 AU ml−1, ega dless o he ype o accine admin-
is e ed and 120 cases (72.29%) ou o accina ed wi h
Mode na and 159 cases (57.19%) ou o accina ed wi h
P ize showed an ibody le els >=1000 AU ml−1. An ibody
le els a 8 mon hs a e accina ion had dec eased o
23.62% and 33.03% in Mode na o P ize accina ed,
espec i ely.
In people younge han 30 yea s, an ibody le els a e
highe compa ed o olde pa ien s (4229 s. 3699) a 8
mon hs and dec ease as e , ega dless o he ype o ac-
cine ecei ed.
DISCUSSION
The eagen s used o he de e mina ion o an i- S and
an i- N an ibodies ha e been e alua ed by a ious au ho s
(B yan e al.,2020; Na asimhan e al.,2021) wi h sa is ac-
o y esul s. In he case o IgG, he ki p o ides quan i a-
i e esul s exp essed in AU ml−1.
P ize accine con e s 95% p o ec ion agains
COVID- 19 (Polack e al.,2020). Simila da a ha e been
showed by o he au ho s (Vasileiou e al.,2021). Mode na
accine has a 94.1% e icacy in p e en ing SARS- CoV- 2
disease, including se e e disease (Baden e al., 2021;
Mahase,2020).
Bo h accines induce he p oduc ion o an ibodies o
he spike (S p o ein) ha co ela e signi ican ly wi h neu-
alizing ac i i y o SARS- CoV- 2 (Wajnbe g e al.,2020).
Bo h ha e been applied o heal hca e wo ke s in Sec o III
o he SALUD in A agon, Spain.
Knowledge o he kine ics o an ibodies induced by
accines agains COVID is impo an o implemen a mo e
app op ia e p e en i e s a egy, especially when accines
may be less e ec i e agains a ian s o he i us (Jang a
e al.,2021).
The Mode na and P ize accines induced an IgG
esponse in 100% o he s udied cases, which is s ill
p esen 2 mon hs a e he second dose, al hough wi h
di e en le els o in ensi y. Mode na accine induces
a highe esponse in e ms o mean IgG concen a ion,
pe cen age o posi i e IgM and a e age IgM index. This
applies o pa ien s wi hou and wi h p e ious in ec ion.
These da a would be consis en wi h hose pub-
lished by se e al au ho s (K amme e al.,2021; Manis y
e al.,2021), who obse ed a signi ican ly highe IgG e-
sponse ollowing P ize accine in pa ien s wi h p e ious
in ec ion. In addi ion, Mon oya e al.(2021) desc ibe sig-
ni ican di e ences in IgG indexes in a ou o Mode na
be ween 42– 48 and 70– 83 days a e he second dose.
In i e cases, all o hem women, om 37 o 55 yea s
old, an i- S1 IgG alues we e less han 1000 AU ml−1, lowe
han he a e age alue o all he heal hca e wo ke s s ud-
ied. Fou o hem had no been p e iously in ec ed and
had numbe s g ea e han 700. The i h had an IgG con-
cen a ion o 200.7AU ml−1: his case had been p e iously
TABLE 4 IgG and IgM esponse in o al popula ion and accine ype in ex- in ec ed pa ien s
Vaccine Pa ien s
IgG an i- S1 IgM an i- S
Posi i e
Mean AU ml−1
(SD) Range Posi i e
Mean index
(SD) Range
Mode na 110 110 (100%) 21,881 (11786) 3335– >40,000 33 (30.00%) 2.62 (2,14) 1.03– 12.13
P ize 131 131 (100%) 15,733 (10310) 200– >40,000 50 (38.16%) 2.98 (2.39) 1.00– 14.93
To al 241 241 (100%) 18,539 (11405) 200– >40,000 83 (34.43%) 2.84 (2.29) 1.00– 14.93
TABLE 5 IgG an i- S1 esponse 8 mon hs a e he second dose o accine
Vaccine Pa ien s Posi i e Mean AU ml−1 (SD) Range
Mode na 166 166 (100%) 4297 (6289) 132– >40,000
P ize 278 278 (100%) 3449 (6645) 120– >40,000
To al 444 444 (100%) 3766 (6519) 120– >40,000
TABLE 6 An ibody le el a ia ion 8 mon hs a e he second
dose o accine
Va ia ion Numbe o cases %
Dec ease 416 93.69
Inc ease 25 5,53
No change 3 0,68
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1973
RESPONSE TO TWO SARS- COV- 2 VACCINES
asymp oma ically in ec ed and wi h an i- N IgG indexes o
5.13 and 4.97 a 11 and 7mon hs p io o sampling, e-
spec i ely, and 5.07 a he ime o se um ex ac ion o his
s udy.
The low pe cen age o IgM posi i e cases 2 mon hs a e
accina ion wi h bo h ypes o accines is su p ising. I is
p obably a ep oduc ion o low IgM esponse a e acci-
na ion wi h apid nega i iza ion o e en wi hou IgM e-
sponse. This is a simila si ua ion o ha desc ibed in 20%
o MERS pa ien s in whom an ibodies a e no de ec ed a
30 days o e olu ion (Co man e al.,2016). In o he s udy,
all pa ien s o med an ibodies, bu 28% we e IgM nega i e
a 2 mon hs (Shi e al.,2004). In he s udy by Na asimhan
e al.(2021) IgM was de ec ed un il day 80, bu wi h oscil-
la ing alues om day 23 wi h a downwa d end.
The IgM esponse has been s onge wi h P ize , in pe -
cen age and mean, in pa ien s who had been in ec ed, bu
wi hou signi ican di e ences. The e may be a bias in he
classi ica ion o cases wi hou p io in ec ion owing o a
sho pe sis ence o an i- N IgG in cases o p e ious in ec-
ion wi h SARS- CoV- 2 (Shang e al.,2021).
These di e ences in he esponse o he immune sys-
em may be ela ed wi h he di e en concen a ion o ac-
cine an igen and adminis a ion egimen, wi h Mode na
100 mic og ams and boos ed 4 weeks a e and wi h P ize
30 mic og ams and boos ed 3 weeks la e .
The s onge esponse wi h Mode na accine, in pa-
ien s wi hou p e ious in ec ion and in p e iously in ec ed
pa ien s, may poin o a g ea e pe sis ence o an ibodies
induced by i and ep esen s g ea e immunop o ec ion.
IgG an ibody le els an i- SARS- CoV2 pe sis a
8 mon hs in all heal hca e wo ke s a e comple e acci-
na ion wi h Mode na o P ize , bu dec easing o 23% and
33%, espec i ely. The as e dec ease o an ibody le els
wi h Mode na could be ela ed wi h a mo e in ense ini ial
esponse. These da a sugges a limi ed pe sis ence o an i-
bodies a e accina ion and he need o e accina ion. In
pa ien s wi h a mild o mode a e disease cou se, immuno-
logical esponse appea s in mos indi iduals and pe sis s
o a leas 10mon hs, al hough bo h IgG an ibody le els
and IFN- γ concen a ions dec eased o abou a hal wi hin
300 days (Schi ne e al.,2021).
In people unde 30 yea s, he an ibody le els we e
highe a e 8 mon hs and diminished as e . I could be
explained because he younge p oduced mo e an ibodies
a e he i s de e mina ion compa ed o he olde be-
cause he immune sys em is less e ec i e as age inc eases.
Mo e s udies a e needed o de e mine he du a ion o
esponse and he le el o p o ec ion, impo an da a o de-
e mine he equency o e accina ion, he an igenic o -
mula ion and he e icacy o accines agains he di e en
a ian s.
AUTHOR CONTRIBUTIONS
L.S., and R.B. designed and coo dina ed he esea ch s ud-
ies, conduc ed expe imen s, analysed da a, and w o e he
i s e sion o he manusc ip ; S.A., J.B., and M.D. con-
duc ed expe imen s; B.H., MT.G., J.M., B.A., A.T., P.S.,
and C.Y. accina ed, go da a and egis e ed he subje s
and ob ained human samples. All au ho s ha e ead and
ag eed o he published e sion o he manusc ip .
ACKNOWLEDGEMENTS
The au ho s wan o pa icula ly acknowledge he e-
c ui ed heal hca e wo ke s o hei collabo a ion.
CONFLICT OF INTEREST
The au ho s decla e no con lic o in e es .
DATA AVAILABILITY STATEMENT
Da a a ailable on eques om he au ho s.
ORCID
C is ina Yus e h ps://o cid.o g/0000-0003-3667-523X
Ra ael Beni o h ps://o cid.o g/0000-0001-5134-1006
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