Since Janua y 2020 Else ie has c ea ed a COVID-19 esou ce cen e wi h
ee in o ma ion in English and Manda in on he no el co ona i us COVID-
19. The COVID-19 esou ce cen e is hos ed on Else ie Connec , he
company's public news and in o ma ion websi e.
Else ie he eby g an s pe mission o make all i s COVID-19- ela ed
esea ch ha is a ailable on he COVID-19 esou ce cen e - including his
esea ch con en - immedia ely a ailable in PubMed Cen al and o he
publicly unded eposi o ies, such as he WHO COVID da abase wi h igh s
o un es ic ed esea ch e-use and analyses in any o m o by any means
wi h acknowledgemen o he o iginal sou ce. These pe missions a e
g an ed o ee by Else ie o as long as he COVID-19 esou ce cen e
emains ac i e.
Li e Sciences 271 (2021) 119200
A ailable online 9 Feb ua y 2021
0024-3205/© 2021 Else ie Inc. All igh s ese ed.
Sc eening o se e e acu e espi a o y synd ome co ona i us-2 in ec ion
du ing labo and deli e y using polyme ase chain eac ion and
immunoglobulin es ing
Rica do Sa i ´
on-Co nudella
a
,
*
, Ana Villalba
a
, Luis M. Es eban
b
, Mau icio Tajada
c
,
Bel´
en Rod íguez-Solanilla
c
, Me cedes Andey o-Ga cia
a
, Ja ie Zapa diel
d
, Segundo Ri e
e
,
Be a Cas ´
an-La az
, Faus ino R. P´
e ez-L´
opez
g
a
Depa men o Obs e ics and Gynecology, Villalba Gene al Uni e si y Hospi al, Mad id, Spain
b
Escuela Uni e si a ia Poli ´
ecnica de La Almunia, Uni e sidad de Za agoza, Za agoza, Spain
c
Depa men o Obs e ics and Gynecology, Miguel Se e Uni e si y Hospi al, Za agoza, Spain
d
Depa men o Mic obiology, Villalba Gene al Uni e si y Hospi al, Mad id, Spain
e
Neona ology Uni , Miguel Se e Uni e si y Hospi al, Za agoza, Spain
Depa men o Obs e ics and Gynecology, San Ped o Hospi al, Log o˜
no, Spain
g
A agon Heal h Resea ch Ins i u e, and Depa men o Obs e ics and Gynecology, Uni e si y o Za agoza Facul y o Medicine, Za agoza, Spain
ARTICLE INFO
Keywo ds:
Co ona i us 2019
COVID-19
Labo and deli e y
Polyme ase chain eac ion
SARS-CoV-2
Se um immunoglobulins
ABSTRACT
Aims: To assess se e e acu e espi a o y synd ome co ona i us-2 (SARS-CoV-2) in ec ion du ing labo and de-
li e y wi h polyme ase chain eac ion (PCR) and using immunoglobulin G and M es ing o co ela e wi h
ma e nal and pe ina al ou comes.
Main me hods: P egnan women admi ed o labo and deli e y a wo Spanish hospi als we e sc eened o SARS-
CoV-2 in ec ion by PCR es and by de ec ion o se um immunoglobulins G and M. Ma e nal and pe ina al
ou comes we e compa ed in women wi h labo a o y e idence o SARS-CoV-2 in ec ion wi h hose wi h nega i e
es s.
Key indings: Be ween Ma ch 31s and Sep embe 30 h, 2020, 1211 p egnan women we e sc eened o SARS-
CoV-2 in ec ion. The p e alence o labo a o y e idence o SARS-CoV-2 in ec ions was 5.4% (n =65), co e-
sponding o (i) 22 ongoing in ec ions a admission, including wo wi h mild clinical symp oms and 20 asymp-
oma ic women; (ii) 43 cases o p e ious SARS-CoV-2 exposu e; (iii) and 1146 women who we e nega i e o
bo h SARS-CoV-2 PCR and se ological es . None o he sc eened mo he s equi ed hospi al admission o
co ona i us disease be o e o a e deli e y, no we e any o he newbo ns admi ed o he in ensi e ca e uni . All
newbo ns om mo he s wi h posi i e PCR on admission we e PCR nega i e. The e we e no signi ican di e -
ences in ma e nal o pe ina al ou comes among he h ee s udied g oups.
Signi icance: Ongoing o p e ious SARS-CoV-2 in ec ion wi h asymp oma ic o mild clinical symp oms de ec ed
du ing sc eening in p egnan women a labo and deli e y do no ha e a highe a e o ad e se ma e nal o
pe ina al ou comes.
1. In oduc ion
Se e e acu e espi a o y synd ome co ona i us 2 (SARS-CoV-2) is
esponsible o he mos apid epidemic in he his o y o humankind. A
he end o Decembe 2020, he Wo ld Heal h O ganiza ion epo ed o e
79.2 million cases and o e 1.7 million dea hs since he s a o he
pandemic [1]. In p egnan women he i al in ec ion has been
associa ed wi h ad e se ou comes [2] and he isk o e ical ans-
mission is a ma e o deba e [3,4]. The i s epo ed cases o his
in ec ion in p egnan women om Wuhan (China) p esen ed wi h
pneumonia, con i med by ches compu ed omog aphy. They we e
ea ed be ween Decembe 2019 and Ma ch 2020, and p esen ed a
posi i e polyme ase chain eac ion (PCR) [5]. Howe e , a la ge p o-
po ion o p egnan women had less se e e o asymp oma ic o ms o he
* Co esponding au ho a : Camino de Mo alza zal M-608 Km, Calle Alped e e 41, 28400 Collado Villalba, Mad id, Spain.
E-mail add esses: [email p o ec ed], [email p o ec ed] (R. Sa i ´
on-Co nudella).
Con en s lis s a ailable a ScienceDi ec
Li e Sciences
jou nal homepage: www.else ie .com/loca e/li escie
h ps://doi.o g/10.1016/j.l s.2021.119200
Recei ed 7 Decembe 2020; Recei ed in e ised o m 1 Feb ua y 2021; Accep ed 3 Feb ua y 2021
Li e Sciences 271 (2021) 119200
2
in ec ion du ing he same pe iod. The e iew o Pe i osso e al. [6]
p o ided in o ma ion om 1287 con i med in ec ions in p egnan
women, including 19 in ec ed neona es. When uni e sal sc eening is
unde aken, he ma e nal asymp oma ic in ec ion a es ange om 43.5
o 92% o cases. I seems ha he a iable numbe o se e e clinical cases
in g a ids could be ela ed o di e ences in i al p e alence among hei
espec i e communi ies.
The sys ema ic e iew by Hun ley e al. [7] o 13 s udies (including
a leas 10 p egnan women wi h SARS-CoV-2 in ec ion) poin ed ou he
low a e o se e e cases, epo ing in ensi e ca e uni admission a 3.0%,
ma e nal c i ical disease a 1.4%, and no ma e nal dea hs. Howe e ,
p e e m bi h and cesa ean deli e y a es a e inc eased and in luenced
by di e en c i ical p ac ices. The ecen me a-analysis by Yee e al. [8]
concluded ha du ing p egnancy, SARS-CoV-2 in ec ion displays ela-
i ely mild symp oms, mo e equen labo a o y pa ame e al e a ions
han in non-p egnan women, a e al SARS-CoV-2 a ec ion o a ound
2%, and a neona al dea h a e o 0.4%. Howe e , new ala ming da a
ha e been epo ed om mac o-s udies on he se e i y o he SARS-CoV-
2 in ec ion and mo ali y in p egnan women, such as he Mexican Na-
ional s udy [9,10].
SARS-CoV-2 sc eening o p egnan women du ing labo and deli e y
has been a widesp ead clinical p ac ice since he beginning o he
pandemic [11,12]. The p e alence o SARS-CoV-2 among his popula-
ion anges om 0.43 o 19.9%, depending on he poin along he
pandemic cu e ( i s wa e, second wa e, o in e wa e pe iod), and
whe e he s udy was ca ied ou [12–15]. In compa ison o non-
p egnan adul s, hal o g a ids wi h SARS-CoV-2 pneumonia display a
no mal ini ial body empe a u e wi h leukocy osis and lymphopenia.
Mo eo e , mixed consolida ion and comple e consolida ion we e com-
mon among labo a o y-con i med cases [3]. High asymp oma ic a es
(43–88%) ha e also been demons a ed among p egnan women
admi ed o labo and deli e y [11,14–17], esembling a es in he non-
p egnan popula ion (86%) [18]. The main diagnos ic ool o he
de ec ion o ongoing in ec ion wi h SARS-CoV-2 has been polyme ase
chain eac ion (PCR).
S udies ha e p oposed he sc eening o SARS-CoV-2 o p egnan
women du ing labo and deli e y, including bo h he PCR and plasma
enzyme-linked immunoso ben assay (ELISA) plasma SARS-CoV-2 G and
M immunoglobulin (Ig) es ing [19,20]. This app oach has been pos u-
la ed o p o ide a much mo e accu a e p e alence han PCR alone. The
main objec i e o he p esen s udy was o assess he alue o combined
PCR and IgG and M de ec ion by se ological es s pe o med du ing labo
and deli e y, and o co ela e esul s wi h ad e se ma e nal (AMOs) and
pe ina al (APOs) ou comes in h ee g oups o p egnan women: (i)
ongoing SARS-CoV-2 in ec ion (posi i e PCR), (ii) p e ious i al in ec-
ion (nega i e PCR wi h posi i e IgG ega dless o IgM), and (iii) no
e idence o in ec ion (asymp oma ic woman wi h bo h nega i e PCR
and nega i e IgM and IgG es s).
2. Me hods
This coho s udy was conduc ed be ween he 31s o Ma ch and 31s
o Sep embe 2020, a he Villalba Gene al Uni e si y Hospi al, Mad id,
and he Miguel Se e Uni e si y Hospi al, Za agoza, Spain. The esea ch
p o ocol was app o ed by he Fundaci´
on Jim´
enez Díaz Clinical Resea ch
E hics Commi ee, Mad id, Spain (P o ocol EO194-20_HGV), and he
Clinical Resea ch E hics Commi ee o A agon (PI 20/508). The STROBE
s a emen o obse a ional s udies was ollowed du ing s udy [21]. A
o al o 1211 p egnan women admi ed o labo and deli e y o
scheduled o labo induc ion o cesa ean deli e y we e sc eened by PCR
using nasopha yngeal swabs and es ing IgG and IgM class an ibodies.
The inclusion c i e ion conside ed p egnancies o e 23 weeks in ges a-
ions wi h spon aneous o induced labo . Exclusion c i e ia co e-
sponded o non-p egnan women, win p egnancies, and neona al o
in au e ine dea hs due o e al mal o ma ions. Th ee pa ien s wi h
nega i e PCR, posi i e IgM and nega i e IgG we e conside ed as possible
alse-posi i e cases and we e excluded ollowing he ecommenda ions
o he Spanish Minis y o Heal h Guidelines [22].
We eco ded he ollowing ma e nal cha ac e is ics: age, pa i y,
hype ensi e diso de s, and p eges a ional and ges a ional diabe es
melli us. Ad e se ma e nal ou comes included in apa um e e , and
hemo hage o pos pa um u e ine a ony. O he symp oms such as
cough, hino hea, dyspnea, ches pain, dia hea, myalgia, new
anosmia, o ageusia we e eco ded, bu wi h no incidence. Obs e ic and
pe ina al da a eco ded o each deli e y co esponded o newbo n sex,
deli e y ( aginal, ins umen al, o cesa ean deli e y), ges a ional age a
bi h, bi h weigh , pe cen ile o he bi h weigh , and a e ial co d
blood pH. We also eco ded he ollowing ad e se pe ina al ou comes:
small o ges a ional age (bi h weigh less han 3 d pe cen ile), 5 min
Apga sco e <7, a e ial co d blood <7.10, ins umen al deli e y o
non- eassu ing e al s a us (NRFS), cesa ean deli e y o NRFS, s ill-
bi h, and neona al In ensi e Ca e Uni (ICU) admission a es.
All he women we e classi ied in o one o he h ee SARS-CoV-2
ca ego ies: (i) ongoing in ec ion (posi i e PCR); (ii) p e ious in ec ion
(nega i e PCR wi h posi i e IgG ega dless o IgM), ollowing he ec-
ommenda ions o he Spanish Minis y o Heal h Guidelines [12]; and
(iii) women wi h no e idence o SARS-CoV-2 in ec ion (nega i e PCR
and nega i e IgG and IgM es s).
2.1. Labo a o y es s
A he Villalba Gene al Uni e si y Hospi al, ELISA se ological IgG and
IgM es ing we e ca ied ou in p egnan women wi h posi i e PCR o
posi i e apid an ibody es . The apid an ibody es is a la e al low
immunoch oma og aphic assay ha uses he Biozek co ona i us 2019
IgG/IgM Rapid Tes Casse e. The ELISA se ological p esence o an i-
bodies was de e mined o G ype wi h Abbo eagen , and o M ype
wi h Vi cell eagen . A he Miguel Se e Uni e si y Hospi al, PCR e-
agen s co esponded o he Xpe Xp ess SARS-CoV-2, Liaison® SARS-
CoV-2 solu ions, and he Viasu e SARS-CoV-2 eal- ime PCR de ec ion
ki . The ELISA se ological p esence o IgM and IgG was de e mined using
he Liaison Diaso in eagen .
2.2. S a is ical analysis
As con inuous a iables did no ollow a no mal dis ibu ion, median
and in e qua ile anges we e calcula ed, and o ca ego ical a iables,
absolu e o ela i e equencies we e epo ed. Compa isons among he
h ee SARS-CoV-2 pa ien ca ego ies (ongoing in ec ion, p e ious
in ec ion, and women wi h no e idence o ongoing o p e ious SARS-
CoV-2 in ec ion) we e pe o med by K uskal-Wallis o chi-squa e es s
o con inuous and ca ego ical a iables. Mo eo e , we pe o med a
wo-by- wo compa ison be ween he g oups: posi i e PCR, nega i e PCR
wi h posi i e IgG ega dless o IgM, and nega i e PCR wi h nega i e
esul s o IgG and IgM an ibodies using Mann-Whi ney o chi-squa ed
es s. Analyses we e pe o med using R e sion 3.6.2 language p o-
g amming (R Founda ion o S a is ical Compu ing, Vienna, Aus ia),
and p- alues <0.05 we e conside ed signi ican .
3. Resul s
Du ing he s udy pe iod s udy, 1211 p egnan women we e admi ed
o labo and deli e y and subjec ed o SARS-CoV-2 sc eening using PCR
and se ological examina ion o an i-SARS-CoV-2 an ibodies (IgG and
IgM; Fig. 1). None o he g a ids we e a ec ed by SARS-CoV-2 pneu-
monia o any o he se e e clinical symp om du ing he s udy pe iod. The
p e alence o SARS-CoV-2 in ec ion was 5.4%, co esponding o 43
p e ious SARS-CoV-2 exposu es and 22 ongoing in ec ions, wo o hem
had co ona i us disease 2019 (COVID-19) symp oms a he ime o
admission, and 10 we e asymp oma ic cases wi hou an ibodies. Bo h
PCR and an ibodies o SARS-CoV-2 we e nega i e in 1146 women.
None o he sc eened mo he s we e admi ed o COVID-19 be o e o
R. Sa i ´
on-Co nudella e al.
Li e Sciences 271 (2021) 119200
3
a e deli e y, no we e any o he newbo ns equi ed o s ay in he
neona al ICU. All newbo ns o 22 mo he s wi h posi i e PCR on
admission we e PCR nega i e. Du ing he s udy pe iod, he e we e no
p egnan women admi ed o he Depa men o In ec ious Diseases o
he In ensi e Ca e Uni s (ICUs).
Table 1 shows he baseline cha ac e is ics o he h ee g oups s ud-
ied: (i) p egnan women wi h ongoing SARS-CoV-2 in ec ion, (ii) p e-
ious i al in ec ion, and (iii) no e idence o in ec ion. We ound
s a is ically signi ican di e ences in ma e nal age (p =0.028), pa i y (p
=0.023), and p eges a ional diabe es melli us (p =0.022) a es. O he
clinical a iables s udied (ch onic hype ension, ges a ional diabe es
melli us, and obs e ic ou comes) did no show signi ican di e ences.
Table 2 displays he ma e nal and pe ina al ad e se ou comes, wi h no
signi ican di e ences among he h ee p ede ined g oups o ma e nal
in apa um e e , pos pa um u e ine hemo hage o a ony, hype en-
si e diso de s o p egnancy, e al g ow h es ic ion, 5-min Apga sco e
<7, a e ial co d blood pH <7.10, ins umen al deli e y o NRFS,
cesa ean deli e y o NRFS, s illbi h and neona al ICU admission. The
Hospi al p o ocols did no include epe i ion o se ological es ing.
The e we e simila esul s in he wo-by- wo compa isons among he
h ee s udied g oups (Table 3), wi h s a is ically signi ican di e ences
in mode o deli e y (p =0.03) in he compa ison o (i) SARS-CoV-2 PCR
nega i e/IgG posi i e e sus; (ii) SARS-CoV-2 PCR nega i e/IgG nega-
i e; and ma e nal age (p =0.015), pa i y (p =0.02), and p eges a ional
diabe es melli us (p =0.008) in he compa ison o (iii) SARS-CoV-2 PCR
posi i e e sus (i ) SARS-CoV-2 PCR nega i e/IgG nega i e. As shown
in Table 3, he e we e no signi ican di e ences among he s udied
g oups o o he a iables: ma e nal age, pa i y, ch onic hype ension,
hype ensi e diso de s o p egnancy, p eges a ional diabe es melli us,
ges a ional diabe es melli us, e e , hemo hage o pos pa um u e ine
a ony, newbo n sex, mode o deli e y, ges a ional age a bi h, bi h and
pe cen ile bi h weigh , a e ial co d blood pH, e al g ow h es ic ion,
5-min Apga sco e <7, a e ial co d blood pH <7.10, ins umen al and
cesa ean deli e y o NRFS, s illbi h and neona al ICU admission.
4. Discussion
O he 1211 p egnan women sc eened o SARS-CoV-2 exposu e, 43
had a p e ious i al exposu e wi h posi i e IgG es , and 1146 women
we e nega i e o bo h PCR and immunoglobulin G and M es s. The
p e alence o SARS-CoV-2 in ec ion in p egnan women was 5.4%.
Du ing he s udy pe iod, none o he women o he newbo ns had
pneumonia o any o he symp oms ha equi ed hei admission o he
in ensi e ca e uni . The e we e no di e ences in ma e nal o neona al
ou comes ac oss he h ee g oups o p egnan women (ongoing in ec-
ion, p e ious in ec ion, and women wi h no e idence o SARS-CoV-2
in ec ion).
A la ge numbe o publica ions du ing he i s wa e o he SARS-
CoV-2 epidemic we e based on se e e o ms o he in ec ion. Howe -
e , he i al in ec ion can display only mild symp oms o e en be
asymp oma ic. Se e al epo s ha e desc ibed sc eening wi h PCR in
p egnan women admi ed o labo and deli e y since he beginning o
he pandemic si ua ion, wi h esul s anging om less han 1% [13,17]
o 15–20% [11,12]. This a iabili y may be due o se e al ac o s,
including di e ences among he s udied popula ions, li es yle, heal h-
ca e sys ems, and ec ui men o s udied women in di e en phases o
Fig. 1. Flowcha o uni e sal sc eening wi h polyme ase chain eac ion (PCR) and immunoglobulins G and M in spon aneous o planned deli e ies (labo induc ion
o cesa ean deli e y).
R. Sa i ´
on-Co nudella e al.
Li e Sciences 271 (2021) 119200
4
he SARS-CoV-2 pandemic. In p egnan women du ing hei i s
imes e , C o e o e al. [20], in Ba celona (Spain), epo ed a highe
p e alence o SARS-CoV-2 by se ological es ing (14%) han by PCR
(0.78%) in 871 women, a ending a i s - imes e sc eening (n =372)
o deli e y (n =502). Ou p elimina y s udy o 266 p egnan women
s udied du ing deli e y in Za agoza (Spain) ound a p e alence o 6.8%
o se ological es s and 2.2% o he PCR p ocedu e [23], whe eas
p e alence o he p esen sample o 1211 women om Mad id and
Za agoza we e 3.6% and 1.8%, espec i ely. Ou se op e alence o
SARS-CoV-2 du ing labo and deli e y is close o he 5.0% epo ed a e
in he main Spanish popula ion [24].
The ma e nal and neona al clinical cou se o ou s udied popula ion
showed simila ma e nal and pe ina al ou comes when compa ing
women wi h and wi hou SARS-CoV-2 in ec ion. P e ious s udies using
only PCR es ing du ing labo and deli e y, in bo h symp oma ic and
asymp oma ic COVID-19 pa ien s, epo ed high a es o cesa ean de-
li e y among hese women [15,16]. In a se ies o 675 p egnan women
om New Yo k admi ed o labo and deli e y, P abhu e al. [15] e-
po ed a sligh inc ease in he a e o cesa ean deli e y in symp oma ic
COVID-19 women (46.7%) compa ed o asymp oma ic ones (45.5%).
Díaz-Co ill´
on e al. [16] in Chile desc ibed ano he s udy o SARS-
CoV-2 in 583 pa ien s using only PCR du ing labo and deli e y
admission. They epo ed a 43.2% a e o asymp oma ic women and no
signi ican di e ences in pe ina al ou comes, bu a end owa ds a
highe a e o p e e m bi h. In ou coho , we had a low a e o cesa ean
deli e ies, and he e we e no di e ences in aginal o cesa ean deli e y
a es among any o he g oups. Howe e , ou a e o symp oma ic SARS-
CoV-2 in ec ions was lowe han hose epo ed in bo h he New Yo k
and Chilean s udies. The e o e, we mus exe cise cau ion when in e -
p e ing he cesa ean sec ion a es and o he ou comes o p egnan
women included in uni e sal PCR sc eening, compa ed o hose o
symp oma ic cases.
Ege up e al. [25] s udied a popula ion o 1313 p egnan women, in
Copenhagen (Denma k), om Ap il o July 2020, including 28 cases o
posi i e an ibodies and one case o posi i e PCR. The s udy concluded
ha SARS-CoV-2 in ec ion was no associa ed wi h obs e ic complica-
ions in p egnan women who had had he disease. In ou s udy wi h 43
IgG posi i e women, we also ound no di e ences in ad e se pe ina al
e ec s be ween he 22 cases wi h posi i e PCR, as compa ed wi h
women no exposed o he SARS-CoV-2 in ec ion. Some au ho s ha e
desc ibed highe p e e m bi h a es associa ed wi h COVID-19 in
p egnan women [26,27]. We did no ind a highe a e o p e e m bi h
in ongoing o p e ious SARS-CoV-2 in ec ions p obably due o he mild
clinical cou se in ou pa ien s, whe eas indings may di e in symp-
oma ic coho s. Ou esul s i well wi h he Flanne y e al. s udy [28]
pe o med in wo cen e s o Philadelphia (Pennsyl ania, US), using bo h
he PCR and se ological es s. They epo ed 80 posi i e se ological es s
in a popula ion o 1293 women o di e en e hnici ies du ing labo and
deli e y, including 6.2% posi i e IgG and/o IgM SARS-CoV-2 women.
This Ame ican s udy, and ou esul s, poin ou he con enience o
s udying IgG and IgM o ob ain mo e p ecise in o ma ion han only
using PCR in pa u ien s a isk o in ec ion by SARS-CoV-2.
The Elsha eey e al. [29] e iew epo ed 95.6% o mild cases in
p egnan women wi h SARS-CoV-2 in ec ion, bu a 4.41% a e o
admission o ma e nal ICU wi h 1.67% equi ing mechanical
Table 1
Ma e nal cha ac e is ics and obs e ic ou comes in h ee g oups o p egnan
women s udied du ing labo and deli e y: (i) p egnan women wi h ongoing
SARS-CoV-2 in ec ion, (ii) p e ious i al in ec ion, and (iii) no e idence o i al
in ec ion. Resul s exp essed as n (pe cen ages) and median (in e qua ile ange).
Posi i e PCR Nega i e PCR
Posi i e IgG
Nega i e PCR
Nega i e IgG
p-
alue
Miguel Se e
Hospi al
13 (73.4) 24 (59.1) 841 (55.8) 0.015
Villalba Gene al
Hospi al
9 (26.6) 19 (40.9) 305 (44.2)
To al p egnan
women
22 (1.8) 43 (3.6) 1146 (94.6)
Ma e nal
cha ac e is ics
Median ma e nal
age
29.2
(24.4–35.4)
33.0
(27.8–36.7)
33.5
(29.6–37.3)
0.028
Pa i y
0 13 (59.1) 19 (44.2) 587 (51.2) 0.023
1 3 (13.6) 13 (30.2) 381 (33.2)
2 2 (9.1) 9 (20.9) 120 (10.5)
≥3 4 (18.2) 2 (4.7) 58 (5.1)
Ch onic
hype ension
0 (0) 0 (0) 15 (1.3) 0.483
P eges a ional
diabe es melli us
1 (4.5) 0 (0) 5 (0.4) 0.022
Ges a ional
diabe es melli us
2 (9.1) 7 (16.3) 172 (15.0) 0.720
Obs e ics ou comes
Newbo n sex
Male 13 (59.1) 17 (39.5) 539 (47.0) 0.324
Female 9 (40.9) 26 (60.5) 607 (53.0)
Mode o deli e y
Vaginal
deli e y
16 (72.7) 38 (88.4) 798 (69.6) 0.129
Ins umen al
deli e y
3 (13.6) 3 (7.0) 192 (16.8)
Cesa ean
deli e y
3 (13.6) 2 (4.7) 156 (13.6)
Ges a ional age
(weeks)
39.6
(38.6–40.7)
39.7
(38.7–40.6)
39.9
(39.0–40.3)
0.976
Bi h weigh
(g ams)
3387
(3032–3700)
3335
(2959–3577)
3260
(2970–3552)
0.484
Bi h weigh
(pe cen ile)
55.0
(29.1–86.6)
54.8
(34.9–75.9)
50.9
(25.9–76.3)
0.493
A e ial co d
blood pH
7.28
(7.23–7.33)
7.27
(7.24–7.32)
7.27
(7.22–7.33)
0.977
Ig: immunoglobulin; PCR: polyme ase chain eac ion.
Table 2
Ad e se ma e nal and pe ina al ou comes (pe cen ages) in h ee g oups o
p egnan women s udied du ing labo and deli e y: (i) g a ids wi h ongoing
co ona i us 2019 in ec ion, (ii) p e ious i al in ec ion, and (iii) no e idence o
i al in ec ion.
Ou comes SARS-
CoV-2
posi i e
PCR
SARS-CoV-2
nega i e PCR
and posi i e
IgG
SARS-CoV-2
bo h nega i e
PCR and IgG
P
Ad e se ma e nal
ou comes
Ma e nal in apa um
e e
0 (0) 3 (7.1) 141 (12.3) 0.151
Hemo hage o
pos pa um u e ine
a ony
1 (5) 0 (0) 27 (2.4) 0.475
Hype ensi e
diso de s o
p egnancy
0 (0) 0 (0) 26 (2.3) 0.481
Ad e se pe ina al
ou comes
Fe al g ow h
es ic ion
(pe cen ile<3)
0 (0) 0 (0) 45 (3.9) 0.271
5-min Apga sco e <
7
0 (0) 0 (0) 7 (0.6) 0.818
A e ial co d blood
pH <7.10
0 (0) 1 (2.3) 32 (2.8) 0.718
Ins umen al deli e y
o NRFS
0 (0) 0 (0) 16 (1.4) 0.631
Cesa ean deli e y o
NRFS
0 (0) 0 (0) 23 (2) 0.514
S illbi h 0 (0) 0 (0) 2 (0.2) 0.944
Neona al in ensi e
ca e uni admission
0 (0) 2 (4.7) 35 (3.1) 0.891
Ig: immunoglobulin; NRFS: non eassu ing e al s a us; PCR: polyme ase chain
eac ion,
R. Sa i ´
on-Co nudella e al.

Li e Sciences 271 (2021) 119200
5
en ila ion. Acco ding o his e iew, he si ua ion may no be as
a o able as i ini ially seemed o p egnan women wi h COVID-19,
al hough included epo s ocused on s udying women wi h symp om-
a ic COVID-19. In s udies on uni e sal sc eening o women admi ed o
labo and deli e y, he igu es a e much mo e eassu ing. Thus, P abhu
e al. [15], in New Yo k, desc ibed a mild cou se o COVID-19 disease
among hei coho o 675 p egnan women, wi h only one case o
admission o he ma e nal ICU. In Chile, Díaz-Co ill´
on e al. [16] e-
po ed a 0.51% admission a e o he ma e nal ICU and mechanical
en ila ion. In ou s udy, we did no ha e se e e COVID-19 cases. All o
ou cases had mild symp oms, and none equi ed admission o he ICU,
acco ding o he Wu e al. disease se e i y cha ac e is ics [30]. I seems
ha SARS-CoV-2 in ec ion du ing p egnancy is less se e e han o he
co ona i us espi a o y in ec ions due o he educed p o-in lamma o y
esponse ha is associa ed wi h a lowe le el cy okine s o m du ing
p egnancy [31], and he low SARS-CoV-2 i e s in co d blood plasma
[32]. Howe e , he ecen Na ional Mexican P ospec i e Coho o
P egnan Women con i ms ha he SARS-CoV-2 in ec ion is associa ed
wi h a highe isk o dea h, in uba ion, and ICU admissions in p egnan
women [10]. These he e ogeneous esul s may be ela ed o he a i-
abili y in SARS-CoV-2 p e alence in di e en wo ld egions, and also in
heal hca e access and quali y, li es yle, and o he ac o s [33–35].
Rega ding he ela ionship be ween SARS-CoV-2 and pe ina al
mo bidi y, cases desc ibed in symp oma ic coho s o p ema u e de-
li e ies ha e been mainly associa ed wi h ia ogenesis, ending he
p egnancy ea ly o main ain ma e nal well-being [5,36,37]. P abhu
e al. [15] and Díaz-Co ill´
on e al. [16] showed no inc ease in ad e se
pe ina al ou comes in ma e nal PCR posi i e cases in uni e sal sc eening
a labo and deli e y. Lingkong Zeng e al. [38] desc ibed a case o
pneumonia in a SARS-CoV-2 in ec ed neona e, al hough hey poin ed
ou ha he symp oms could ha e been due o p ema u i y, asphyxia, o
sepsis, a he han o SARS-CoV-2 in ec ion. In ou s udy popula ion, he
ma e nal and pe ina al ou comes we e no signi ican ly di e en be-
ween p egnan women wi h and hose wi hou SARS-CoV-2 in ec ion
al hough, as p e iously men ioned, none o hese women had pneu-
monia o o he clinical symp oms.
The isk o e ical ansmission o SARS-CoV2 du ing labo and
deli e y is s ill no clea [6]. Some esul s sus ain ha he e is li le
e idence o he SARS-CoV-2 e ical ansmission [39]. Howe e , he e
a e also some epo s o asymp oma ic posi i e SARS-COV-2 PCRs in he
newbo ns o in ec ed mo he s [16,38,40]. Yee e al. [8] epo ed i e
neona es wi h posi i e swab es s ha could ha e become in ec ed
du ing aginal o cesa ean deli e y. A ecen me a-analysis calcula ed a
5.3% a e o e ical ansmission and a posi i e SARS-CoV-2 es a e o
8% in neona es om mo he s wi h COVID-19 [41]. Howe e , Alga oba
e al. [42] ecen ly epo ed he p esence o SARS-CoV-2 in he placen a,
using elec on mic oscopy, in a g a id wi h pneumonia ea ed wi h
co icos e oids o e al lung ma u i y be o e a p e e m cesa ean
deli e y.
Pe ina al esul s a e eassu ing, and no neona al complica ions we e
associa ed wi h ma e nal SARS-COV-2 in ec ion in p e ious s udies
[15,16]. Ege up e al. [25] also ound no di e ences be ween pa ien s
wi h posi i e e sus nega i e an ibodies in neona al complica ions. We
ound no signi ican di e ences in APOs among ou h ee g oups, and
none o he neona al in ec ions we e by SARS-CoV-2. Ou s udy is a la ge
coho s udied o e se e al mon hs a wo ins i u ions o he Spanish
Na ional Heal h Sys em ha p o ide heal hca e o he en i e popula ion.
We acknowledge ha ou s udy has some limi a ions. Fi s ly, some
women may ha e omi ed epo ing symp oms because o hei ea o
he implica ions o ha ing a co ona i us in ec ion. Ano he limi a ion is
he small numbe o in ec ed women o epo ep esen a i e esul s o
bo h ma e nal and pe ina al ad e se ou comes, al hough ou esul s a e
in line wi h simila da a. Rega ding he p egnan women wi h a p e ious
in ec ion, we we e unable o de e mine when he in ec ion migh ha e
occu ed, and we did no know i his in luenced he ou comes o he
p egnancy. Mo eo e , he de ec ion ki s used in bo h hospi als we e
om di e en b ands, so could ha e had di e en sensi i i ies and
speci ici ies. Finally, ou s udy is an obse a ional clinical esea ch, and
we acknowledge ha bo h alse posi i e and nega i e esul s may be
possible.
5. Conclusion
P egnan women wi h asymp oma ic SARS-CoV-2 in ec ion o wi h
mild clinical symp oms de ec ed a labo and deli e y do no ha e
highe a es o ad e se ma e nal o pe ina al ou comes han women
wi h nega i e PCR and immunoglobulin es s. The key o ma e nal o
pe ina al ad e se e ec s is he clinical se e i y o SARS-CoV-2 in ec ion
in he p egnan woman. We p o ide e idence ha he s udied neona es
we e no in ec ed in he u e us o du ing deli e y.
Table 3
S a is ical signi icance (p alue) o di e en compa isons o p egnan women
SARS-CoV-2 acco ding o polyme ase chain eac ion (PCR) posi i e/nega i e
and immunoglobulin (Ig) G posi i e/nega i e in h ee g oups o p egnan
women du ing labo and deli e y epo ed by p- alues o Wilcoxon es
compa isons.
SARS-CoV-2 PCR
posi i e e sus
bo h nega i e
PCR and IgG
SARS-CoV-2 PCR
nega i e and IgG
posi i e e sus
PCR nega i e and
IgG nega i e
SARS-CoV-2
PCR posi i e
e sus
PCR nega i e
and IgG
posi i e
Ma e nal ou comes
Ma e nal age (yea s) 0.015 0.245 0.254
Pa i y 0.020 0.194 0.094
Como bidi ies
Ch onic
hype ension
0.589 0.450 0.999
Hype ensi e
diso de s o
p egnancy
0.475 0.318 0.999
P eges a ional
diabe es melli us
0.008 0.664 0.156
Ges a ional diabe es
melli us
0.440 0.819 0.427
Fe e 0.079 0.293 0.204
Hemo hage o
pos pa um u e ine
a ony
0.506 0.308 0.158
Obs e ic ou comes
Newbo n sex 0.364 0.417 0.217
Mode o deli e y 0.925 0.030 0.265
Ges a ional age a
bi h (weeks)
0.892 0.877 0.708
Bi h weigh (g ams) 0.329 0.465 0.713
Pe cen ile bi h
weigh
0.356 0.439 0.731
A e ial co d blood
pH
0.828 0.992 0.906
Pa hological indings p- alue p- alue p- alue
Fe al g ow h
es ic ion
(pe cen ile <3)
0.343 0.185 0.999
5-min Apga sco e <
7
0.713 0.611 0.999
A e ial co d blood
pH <7.10
0.426 0.872 0.487
Ins umen al
deli e y o NRFS
0.402 0.247 0.999
Cesa ean deli e y
o NRFS
0.502 0.353 0.999
S illbi h 0.844 0.786 0.999
Neona al ICU
admission
0.404 0.533 0.298
NRFS: non eassu ing e al s a us.
R. Sa i ´
on-Co nudella e al.
Li e Sciences 271 (2021) 119200
6
CRediT au ho ship con ibu ion s a emen
RSC, AV, LME and FRPL con ibu ed o he concep ion o he s udy.
RSC, LME, FRPL and BCL con ibu ed o he design o he clinical wo k.
RSC, AV, MT, BRS, MAG, JZ and SR ca ied ou da a acquisi ion. LME
and FRPL pe o med s a is ical analyses. All au ho s we e in ol ed in
he in e p e a ion o he s udy esul s, as well as he d a ing and e i-
sion o he manusc ip . All app o ed he inal e sion o be published.
Decla a ion o compe ing in e es
This esea ch did no ecei e a speci ic g an om unding agencies
in he public, comme cial, o no - o -p o i sec o s. The au ho s decla e
ha he e a e no con lic s o in e es .
Acknowledgemen
We g a e ully hank all he s a a Villalba Gene al Uni e si y Hospi al,
Mad id, and a Miguel Se e Uni e si y Hospi al, Za agoza, Spain who
ha e ough agains he SARS-CoV-2 epidemic.
Funding
This esea ch did no ecei e any g an om unding agencies.
Re e ences
[1] Wo ld Heal h O ganiza ion, Weekly Epidemiological Upda e on COVID-19 1,
Wo ld Heal. O gan, 2020, p. 4. h ps://www.who.in /docs/de aul sou ce/co o
na i use/si ua ion- epo s/20201012-weekly-epi-upda e-9.pd .
[2] J. Allo ey, E. S allings, M. Bone , M. Yap, S. Cha e jee, T. Kew, L. Debenham, A.
C. Lla all, A. Dixi , D. Zhou, R. Balaji, S.I. Lee, X. Qiu, M. Yuan, D. Cooma , M. Van
Wely, E. Van Leeuwen, E. Kos o a, H. Kuns , A. Khalil, S. Tibe i, V. B izuela,
N. B ou e , E. Ka a, C.R. Kim, A. Tho son, O.T. Oladapo, L. Mo enson, J. Zamo a,
S. Thanga a inam, Clinical mani es a ions, isk ac o s, and ma e nal and pe ina al
ou comes o co ona i us disease 2019 in p egnancy: li ing sys ema ic e iew and
me a-analysis, BMJ (2020) 370, h ps://doi.o g/10.1136/bmj.m3320.
[3] P. Li, M. Xie, W. Zhang, Clinical cha ac e is ics and in au e ine e ical
ansmission po en ial o co ona i us disease 2019 in ec ion in 9 p egnan women:
a e ospec i e e iew o medical eco ds, Am. J. Obs e . Gynecol. 223 (2020)
955–956, h ps://doi.o g/10.1016/j.ajog.2020.08.059.
[4] S.A. Rasmussen, J.C. Smulian, J.A. Lednicky, T.S. Wen, D.J. Jamieson, Co ona i us
disease 2019 (COVID-19) and p egnancy: wha obs e icians need o know, Am. J.
Obs e . Gynecol. 222 (2020) 415–426, h ps://doi.o g/10.1016/j.
ajog.2020.02.017.
[5] L. Chen, Q. Li, D. Zheng, H. Jiang, Y. Wei, L. Zou, L. Feng, G. Xiong, G. Sun,
H. Wang, Y. Zhao, J. Qiao, Clinical cha ac e is ics o p egnan women wi h Co id-
19 in Wuhan, China, N. Engl. J. Med. 382 (2020), e100, h ps://doi.o g/10.1056/
NEJMc2009226.
[6] E. Pe i osso, M. Giles, S. Cole, M. Rees, COVID-19 and p egnancy: a e iew o
clinical cha ac e is ics, obs e ic ou comes and e ical ansmission, Aus . New
Zeal. J. Obs e . Gynaecol. 60 (2020) 640–659, h ps://doi.o g/10.1111/ajo.13204.
[7] B.J.F. Hun ley, E.S. Hun ley, D. Di Mascio, T. Chen, V. Be ghella, S.P. Chauhan,
Ra es o ma e nal and pe ina al mo ali y and e ical ansmission in p egnancies
complica ed by se e e acu e espi a o y synd ome co ona i us 2 (SARS-co-V-2)
in ec ion: a sys ema ic e iew, Obs e . Gynecol. 136 (2020) 303–312, h ps://doi.
o g/10.1097/AOG.0000000000004010.
[8] J. Yee, W. Kim, J.M. Han, H.Y. Yoon, N. Lee, K.E. Lee, H.S. Gwak, Clinical
mani es a ions and pe ina al ou comes o p egnan women wi h COVID-19: a
sys ema ic e iew and me a-analysis, Sci. Rep. 10 (2020) 1–7, h ps://doi.o g/
10.1038/s41598-020-75096-4.
[9] R.J. Ma inez-Po illa, A. So i iadis, C. Cha zakis, J. To es-To es, S. Espinoy Sosa,
K. Sando al-Mandujano, D.A. Cas o-Be nabe, V. Medina-Jimenez, J.C. Mona ez-
Ma in, F. Figue as, L.C. Poon, P egnan women wi h SARS-CoV-2 in ec ion a e a
highe isk o dea h and se e e pneumonia: p opensi y sco e-ma ched analysis o a
na ionwide p ospec i e coho s udy (COV19Mx), Ul asound Obs e . Gynecol.
(2020), h ps://doi.o g/10.1002/uog.23575.
[10] R.J. Ma inez-Po illa, E.R. Smi h, S. He, J. To es-To es, S. Espino-Y-Sosa, J.
M. Solis-Pa edes, L.C. Poon, Young p egnan women a e also a an inc eased isk o
mo ali y and se e e illness due o co ona i us disease 2019: analysis o he
Mexican Na ional Su eillance P og am, Am. J. Obs e . Gynecol. (2020)
2019–2021, h ps://doi.o g/10.1016/j.ajog.2020.12.1197.
[11] D. Su on, K. Fuchs, M. D’Al on, D. Go man, Uni e sal sc eening o SARS-CoV-2
in women admi ed o deli e y, N. Engl. J. Med. 382 (2020) 2163–2164, h ps://
doi.o g/10.1056/NEJMc2009316.
[12] W.S. Vin zileos, J. Musca , E. Ho mann, N.S. John, R. Ve ichio, A.M. Vin zileos,
D. Vo, Sc eening all p egnan women admi ed o labo and deli e y o he i us
esponsible o co ona i us disease 2019, Am. J. Obs e . Gynecol. (2020), h ps://
doi.o g/10.1016/j.ajog.2020.04.024.
[13] M.J. Fasse , L.D. Lu ey, L. Yasumu a, M. Nguyen, J.J. Colli, M. Voloda skiy, J.
C. Gulle , D. B aun, A. Fong, N. T i edi, K. B ux oo , V. Chiu, D. Ge ahun,
Uni e sal SARS-Co -2 sc eening in women admi ed o deli e y in a la ge
managed ca e o ganiza ion, Am. J. Pe ina ol. 90034 (2020), h ps://doi.o g/
10.1055/s-0040-1714060.
[14] D. Ceulemans, I. Thijs, A. Sch eu s, J. Ve cammen, L. Lannoo, J. Dep es ,
J. Rich e , L. De Ca e, R. De liege , Sc eening o COVID-19 a childbi h: is i
e ec i e? Ul asound Obs e . Gynecol. 56 (2020) 113–114, h ps://doi.o g/
10.1002/uog.22099.
[15] M. P abhu, K. Cagino, K.C. Ma hews, R.L. F iedlande , S.M. Glynn, J.M. Kubiak, Y.
J. Yang, Z. Zhao, R.N. Bae gen, J.I. DiPace, A.S. Raza i, D.W. Skupski, J.R. Snyde ,
H.K. Singh, R.B. Kalish, C.M. Ox o d, L.E. Riley, P egnancy and pos pa um
ou comes in a uni e sally es ed popula ion o SARS-CoV-2 in New Yo k Ci y: a
p ospec i e coho s udy, BJOG An In . J. Obs e . Gynaecol. (2020), h ps://doi.
o g/10.1111/1471-0528.16403.
[16] P. Díaz-Co ill´
on, M. M¨
onckebe g, A. Ba os, S.E. Illanes, A. Solda i, J.K. Nien,
M. Schepele , J. Ca adeux, Rou ine sc eening o SARS CoV-2 in unselec ed
p egnan women a deli e y, PLoS One 15 (2020) 1–13, h ps://doi.o g/10.1371/
jou nal.pone.0239887.
[17] I. He aiz, D. Folguei a, C. Villalaín, L. Fo c´
en, R. Delgado, A. Galindo, Uni e sal
sc eening o SARS-CoV-2 be o e labo admission du ing Co id-19 pandemic in
Mad id, J. Pe ina . Med. 0 (2020), h ps://doi.o g/10.1515/jpm-2020-0236.
[18] R. Li, S. Pei, B. Chen, Y. Song, T. Zhang, W. Yang, J. Shaman, Subs an ial
undocumen ed in ec ion acili a es he apid dissemina ion o no el co ona i us
(SARS-CoV-2), Science (80-.) 368 (2020) 489–493, h ps://doi.o g/10.1126/
science.abb3221.
[19] J. Z¨
ollkau, M. Baie , A. Sche ag, E. Schleußne , T. G o en, Pe iodenp ¨
a alenz on
SARS-CoV-2 in eine unselek ie en S ichp obe schwange e F auen in Jena,
Thü ingen. TT - [Pe iod P e alence o SARS-CoV-2 in an Unselec ed Sample o
P egnan Women in Jena, Thu ingia], Z. Gebu shil e Neona ol. 224 (2020)
194–198, h ps://doi.o g/10.1055/a-1206-1033.
[20] F. C o e o, F. C ispi, E. Llu ba, F. Figue as, M.D. G´
omez-Roig, E. G a ac´
os,
Se op e alence and p esen a ion o SARS-CoV-2 in p egnancy, Lance 396 (2020)
530–531, h ps://doi.o g/10.1016/S0140-6736(20)31714-1.
[21] E. Von Elm, D.G. Al man, M. Egge , S.J. Pocock, P.C. Gø zsche, J.
P. Vandenb oucke, The s eng hening he epo ing o obse a ional s udies in
epidemiology (STROBE) s a emen : guidelines o epo ing obse a ional s udies,
PLoS Med. 4 (2007) 1623–1627, h ps://doi.o g/10.1371/jou nal.pmed.0040296.
[22] Minis e io de Sanidad, Gobie no de Espa˜
na, In e p e aci´
on de las p uebas
diagn´
os icas en e a SARS-CoV-2, e si´
on 2. Ap obado po la Ponencia de Ale as,
P epa aci´
on y Respues a COLABORACI´
ON Sociedad espa˜
nola de En e medades
In ecciosas y Mic obiología Clínica, n.d. h ps://www.mscbs.gob.es/p o esionales/
saludPublica/ccayes/ale asAc ual/nCo /documen os/INTERPRETACION_DE
_LAS_PRUEBAS.pd , 2020. (Accessed 24 Ap il 2020).
[23] R. Sa i ´
on-Co nudella, A. Villalba, J. Zapa diel, M. Andey o-Ga cia, L.M. Es eban,
F.R. P´
e ez-L´
opez, Se e e acu e espi a o y synd ome co ona i us 2 (SARS-CoV-2)
uni e sal sc eening in g a ids du ing labo and deli e y, Eu . J. Obs e . Gynecol.
Rep od. Biol. 256 (2021) 400–404, h ps://doi.o g/10.1016/j.ejog b.2020.11.069.
[24] M. Poll´
an, B. P´
e ez-G´
omez, R. Pas o -Ba iuso, J. O eo, M.A. He n´
an, M. P´
e ez-
Olmeda, J.L. Sanma ín, A. Fe n´
andez-Ga cía, I. C uz, N. Fe n´
andez de La ea,
M. Molina, F. Rod íguez-Cab e a, M. Ma ín, P. Me ino-Amado , J. Le´
on Paniagua,
J.F. Mu˜
noz-Mon al o, F. Blanco, R. Yo i, R. Gu i´
e ez Fe n´
andez, S. Mezcua
Na a o, J.F. Mu˜
noz-Mon al o, M. Saline o He n´
andez, J.L. Sanma ín, M. Cuenca-
Es ella, J. Le´
on Paniagua, P. Fe n´
andez-Na a o, A. A ell´
on, G. Fedele, J. O eo
Iglesias, M.T. P´
e ez Olmeda, M.E. Fe nandez Ma inez, F.D. Rod íguez-Cab e a, M.
A. He n´
an, S. Pad ones Fe n´
andez, J.M. Rumbao Agui e, J.M. Na a o Ma í,
B. Palop Bo ´
as, A.B. P´
e ez Jim´
enez, M. Rod íguez-Iglesias, A.M. Cal o Gasc´
on, M.
L. Lou Alcaine, I. Dona e Su´
a ez, O. Su´
a ez ´
Al a ez, M. Rod íguez P´
e ez, M. Cases
Sanchís, C.J. Villa ´
a ila Gomila, L. Ca bo Salad igas, A. Hu ado Fe n´
andez,
A. Oli e , E. Cas o Feliciano, M.N. Gonz´
alez Quin ana, J.M. Ba asa Fe n´
andez, M.
A. He n´
andez Be anco , M. He n´
andez Febles, L. Ma ín Ma ín, L.M. L´
opez L´
opez,
T. Uga e Mio a, I. De Beni o Poblaci´
on, M.S. Celada P´
e ez, M.N. Vall´
es Fe n´
andez,
T. Ma ´
e En íquez, M. Villa A anz, M. Domínguez-Gil Gonz´
alez, I. Fe n´
andez-Na al,
G. Megías Lob´
on, J.L. Mu˜
noz Bellido, P. Ci uela, A. Mas i Casals, M. Dolad´
e Bo ías,
M.A. Ma cos Maeso, D. P´
e ez del Campo, A. F´
elix de Cas o, R. Lim´
on Ramí ez, M.
F. Elías Re amosa, M. Rubio Gonz´
alez, M.S. Blanco Lobei as, A. Fuen es Losada,
A. Aguile a, G. Bou, Y. Ca o, N. Ma au i, L.M. So ia Blanco, I. del Cu a Gonz´
alez,
M. He n´
andez Pascual, R. Alonso Fe n´
andez, N. Cab e a Cas o, A. Tom´
as Lizcano,
C. Ramí ez Almag o, M. Sego ia He n´
andez, N. Ascunce Elizaga, M. Ede a Sanz,
C. Ezpele a Baquedano, A. Bus induy Basca an, S. Iglesias Tamayo, L. Elo duy
O azua, R. Bena och Bena och, J. Lope a Flo es, A. V´
azquez de la Villa,
P e alence o SARS-CoV-2 in Spain (ENE-COVID): a na ionwide, popula ion-based
se oepidemiological s udy, Lance (2020), h ps://doi.o g/10.1016/S0140-6736
(20)31483-5.
[25] P. Ege up, L. Fich Olsen, A.-M.H. Ch is iansen, D. Wes e gaa d, E.R. Se e insen, K.
V.R. H iid, A.M. Kol e, A.D. Boje, M.-L.M.F. Be elsen, L. P æ o ius, A. Zedele , J.
R. Nielsen, D. Bang, S. Be n sen, J. E helbe g-Findsen, D.M. S o m, J. Bello-
Rod íguez, A. Ingham, J. Oll´
e-L´
opez, E.R. Ho mann, C. Wilken-Jensen, L. K ebs, F.
S. Jø gensen, H. Wes h, H.L. Jø gensen, N. la Cou F eiesleben, H.S. Nielsen, Se e e
acu e espi a o y synd ome co ona i us 2 (SARS-CoV-2) an ibodies a deli e y in
women, pa ne s, and newbo ns, Obs e . Gynecol. Publish Ah (2020) 1–7, h ps://
doi.o g/10.1097/aog.0000000000004199.
[26] R. Ma a , L. Al ahmani, N. Monze , L.G. Debiane, E. Be ba i, J. Fa es,
F. Fi zpa ick, M.H. Mu ad, Clinical p esen a ion and ou comes o p egnan women
R. Sa i ´
on-Co nudella e al.
Li e Sciences 271 (2021) 119200
7
wi h co ona i us disease 2019: a sys ema ic e iew and me a-analysis, Clin. In ec .
Dis. (2020) 1–13, h ps://doi.o g/10.1093/cid/ciaa828.
[27] J. Zhao, Q. Yuan, H. Wang, W. Liu, X. Liao, Y. Su, X. Wang, J. Yuan, T. Li, J. Li,
S. Qian, C. Hong, F. Wang, Y. Liu, Z. Wang, Q. He, Z. Li, B. He, T. Zhang, Y. Fu,
S. Ge, L. Liu, J. Zhang, N. Xia, Z. Zhang, An ibody esponses o SARS-CoV-2 in
pa ien s o no el co ona i us disease 2019, Clin. In ec . Dis. (2020), h ps://doi.
o g/10.1093/cid/ciaa344.
[28] D.D. Flanne y, S. Gouma, M.B. Dhudasia, S. Mukhopadhyay, M.R. P ei e , E.
C. Wood o d, J.S. Ge be , C.P. A e alo, M.J. Bol on, M.E. Wei ick, E.C. Goodwin, E.
M. Ande son, A.R. G eenpla e, J. Kim, N. Han, A. Pa eka , J. Doughe y,
O. Ku hu u, D. Ma hew, A.E. Bax e , L.A. Vella, J.E. Wea e , A. Ve ma, R. Lei e, J.
S. Mo is, D.J. Rade , M.A. Elo i z, E.J. Whe y, K.M. Puopolo, S.E. Hensley, SARS-
CoV-2 se op e alence among pa u ien women in Philadelphia, Sci. Immunol. 5
(2020) 1–7, h ps://doi.o g/10.1126/SCIIMMUNOL.ABD5709.
[29] F. Elsha eey, R. Magdi, N. Hindi, M. Elshebiny, N. Fa ag, S. Mahdy, M. Sabbou ,
S. Geb il, M. Nasse , M. Kamel, A. Ami , M. Mahe Ema a, A. Nabhan, A sys ema ic
scoping e iew o COVID-19 du ing p egnancy and childbi h, In . J. Gynecol.
Obs e . 150 (2020) 47–52, h ps://doi.o g/10.1002/ijgo.13182.
[30] Z. Wu, J.M. McGoogan, Cha ac e is ics o and impo an lessons om he
co ona i us disease 2019 (COVID-19) ou b eak in China: summa y o a epo o
72314 cases om he Chinese Cen e o Disease Con ol and P e en ion, JAMA - J.
Am. Med. Assoc. 323 (2020) 1239–1242, h ps://doi.o g/10.1001/
jama.2020.2648.
[31] T. Ghi, E. di Pasquo, A. Mekinian, L. Calza, T. F usca, Sa s-CoV-2 in p egnancy:
why is i be e han expec ed? Eu . J. Obs e . Gynecol. Rep od. Biol. 252 (2020)
476–478, h ps://doi.o g/10.1016/j.ejog b.2020.07.025.
[32] A.G. Edlow, J.Z. Li, A.R.Y. Collie , C. A yeo, K.E. James, A.A. Boa in, K.J. G ay, E.
A. Bo d , L.L. Shook, L.M. Yonke , A. Fasano, K. Diou , N. C oul, S. De ane, L.
J. Yockey, R. Lima, J. Shui, J.D. Ma u e, P.H. Le ou, B.O. Akinwunmi, A. Schmid ,
J. Feldman, B.M. Hause , T.M. Ca adonna, D. De la Flo , P. D’A ino, J. Regan,
H. Co y, K. Coxen, J. Fajnzylbe , D. Pepin, M.S. Seaman, D.H. Ba ouch, B.
D. Walke , X.G. Yu, A.J. Kaimal, D.J. Robe s, G. Al e , Assessmen o ma e nal and
neona al SARS-CoV-2 i al load, T ansplacen al an ibody ans e , and placen al
pa hology in p egnancies du ing he COVID-19 pandemic, JAMA Ne w. Open 3
(2020), e2030455, h ps://doi.o g/10.1001/jamane wo kopen.2020.30455.
[33] Y. A sha , S.L. Gaw, V.J. Flahe man, B.D. Chambe s, D. K akow, V. Be ghella, A.
A. Shamshi saz, A.A. Boa in, G. Ald o andi, A. G eine , L. Riley, W.J. Bosca din, D.
J. Jamieson, V.L. Jacoby, Clinical p esen a ion o co ona i us disease 2019
(COVID-19) in p egnan and ecen ly p egnan people, Obs e . Gynecol. 136
(2020) 1117–1125, h ps://doi.o g/10.1097/AOG.0000000000004178.
[34] F.R. P´
e ez-L´
opez, R. Sa i ´
on-Co nudella, P. Ched aui, A.R. Genazzani, Se e e acu e
espi a o y synd ome co ona i us 19 and human p egnancy, Gynecol. Endoc inol.
36 (2020) 277–278, h ps://doi.o g/10.1080/09513590.2020.1747426.
[35] R. Sa i ´
on-Co nudella, I.E. Al ami ano-Ba cia, P. Ched aui, M. Andey o-Ga cía, M.
C. Tajada-Duaso, F.R. P´
e ez-L´
opez, Co ona i us Disease 2019 (COVID-19) and
Human P egnancy: A Scoping Re iew 1, Gynecological and Rep oduc i e
Endoc inology and Me abolism, 2020, pp. 70–75.
[36] C. Elwood, I. Boucoi an, J. VanSchalkwyk, D. Money, M. Yudin, V. Poliquin, SOGC
commi ee opinion – COVID-19 in p egnancy, J. Obs e . Gynaecol. Canada. (2020),
h ps://doi.o g/10.1016/j.jogc.2020.03.012.
[37] D. Di Mascio, A. Khalil, G. Saccone, G. Rizzo, D. Buca, M. Libe a i, J. Vecchie ,
L. Nappi, G. Scambia, V. Be ghella, F. D’An onio, Ou come o co ona i us
spec um in ec ions (SARS, MERS, COVID-19) du ing p egnancy: a sys ema ic
e iew and me a-analysis, Am. J. Obs e . Gynecol. MFM. 2 (2020), 100107,
h ps://doi.o g/10.1016/j.ajogm .2020.100107.
[38] L. Zeng, S. Xia, W. Yuan, K. Yan, F. Xiao, J. Shao, W. Zhou, Neona al ea ly-onse
in ec ion wi h SARS-CoV-2 in 33 neona es bo n o mo he s wi h COVID-19 in
Wuhan, China, JAMA Pedia . 174 (2020) 722, h ps://doi.o g/10.1001/
jamapedia ics.2020.0878.
[39] G.A. Ryan, N.C. Pu anda e, F.M. McAuli e, M. Hod, C.N. Pu anda e, Clinical
upda e on COVID-19 in p egnancy: a e iew a icle, J. Obs e . Gynaecol. Res. 46
(2020) 1235–1245, h ps://doi.o g/10.1111/jog.14321.
[40] L. Dong, J. Tian, S. He, C. Zhu, J. Wang, C. Liu, J. Yang, Possible e ical
ansmission o SARS-CoV-2 om an in ec ed mo he o he newbo n, JAMA 10
(2020) 49–61, h ps://doi.o g/10.1001/jama.2020.4621.
[41] M. Ja a i, A. Po mohammad, S.A. Sheikh Neshin, S. Gho bani, D. Bose,
S. Alimohammadi, S. Basi ja a i, M. Mohammadi, C. Rasmussen-I ey, M.
H. Razizadeh, M. Nou i-Vaskeh, M. Za ei, Clinical cha ac e is ics and ou comes o
p egnan women wi h COVID-19 and compa ison wi h con ol pa ien s: a
sys ema ic e iew and me a-analysis, Re . Med. Vi ol. (2021), h ps://doi.o g/
10.1002/ m .2208.
[42] G.N. Alga oba, N.N. Hanna, P. Rekawek, S.A. Vahanian, P. Khulla , T. Palaia, M.
R. Pel ie , M.R. Cha ez, A.M. Vin zileos, Con i ma o y e idence o he
isualiza ion o se e e acu e espi a o y synd ome co ona i us 2 in ading he
human placen a using elec on mic oscopy, Am. J. Obs e . Gynecol. 223 (2020)
953–954, h ps://doi.o g/10.1016/j.ajog.2020.08.106.
R. Sa i ´
on-Co nudella e al.