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Fetal pulmonary and cerebral artery Doppler
velocimetry in normal and high risk pregnancy
Tętniczy przepływ krwi w płucach i OUN płodu w ciąży o przebiegu
prawidłowym i w ciąży wysokiego ryzyka
$QGU]HM%UĊERURZLF]1, Mariusz Dubiel2, MareN 3ieWr\Ja,
*rzeJRrz + %rĊbRrRZiFz, 6aePuQGur *uGPuQGssRQ
1
Division of Reproductive Endocrinology and Infertility, Department of Ob/Gyn & Women’s Health – Montefiore Medical Center
Albert Einstein College of Medicine, New York, USA
2
Department of Obstetrics and Gynecology, Collegium Medicum, Nicolaus Copernicus University, Torun, Poland
3
Department of Obstetrics and Women Diseases, Poznań University School of Medical Sciences, Poznań, Poland
4
Department of Perinatology and Gynecology, Poznań University School of Medical Sciences, Poznań, Poland
5
Department of Obstetrics and Gynecology, Malmö University Hospital, Malmö, Sweden
Abstract
Studies on fetal lung/brain circulation by means of power Doppler technique have suggested a marked reduction in
lung perfusion in high-risk pregnancies as a sign of circulation redistribution. The ratio between lung/brain perfusion
might therefore give a new method to predict fetal circulation centralization.
Objective: The aim of the present study was to obtain fetal lung and cerebral artery ratio in normal and high-risk
pregnancies.
Study design: Doppler samples from proximal right pulmonary artery blood velocities and middle cerebral artery
(MCA) were recorded cross-sectionally in 228 normal singleton pregnancies at gestational age 22 to 40 weeks.
MCA / right pulmonary artery pulsatility index (PI) ratio was calculated. Doppler samples from proximal right pulmonary artery and MCA were also recorded in 89 high-risk singleton pregnancies and the results related to perinatal
outcome.
Results: In the normal controls, right pulmonary artery PI remained stable until 30 weeks of gestation with slight
increase thereafter until term. The MCA to right pulmonary artery PI ratio increased between 22 and 28 weeks of
gestation with the rapid fall towards term. In the high-risk pregnancies group, right pulmonary artery PI showed no
significant correlation to perinatal outcome, but signs of brain-sparing in the MCA were correlated to all adverse
outcome parameters.
Conclusion: Velocimetry of the middle cerebral artery is better than velocimetry of right pulmonary artery in predicting adverse outcome of pregnancy. The brain/lung PI ratio does not improve the prediction of adverse outcome
of pregnancy.
Address for correspondence:
Grzegorz H. Bręborowicz
Department of Perinatology and Gynecology, Poznań University School of Medical Sciences
ul. Polna 33, 60 535 Poznań, Poland
tel./fax: +48 61 84 19 283
e-mail: [email protected]
26
© Polskie Towarzystwo Ginekologiczne
Otrzymano: 18.08.2013
Zaakceptowano do druku: 30.10.2013
Nr 1/2014
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O R Y G I N A L N E
po ł o ż n i c t wo
Bręborowicz A, et al. Fetal pulmonary and cerebral artery Doppler velocimetry in normal and high risk pregnancy.
Key words: pulmonary artery / middle cerebral artery / brain-sparing / fetus /
/ Doppler / pregnancy /
Streszczenie
Wstęp: Ocena przepływu krwi przy pomocy metod ddopplerowskich w krążeniu płucnym I mózgowym sugerowała
istotny spadek perfuzji płuc w ciążach wysokiego ryzyka jako wykładnik zmienionej redystrybucji krwi w ustroju płodu. Stworzyło to koncepcję z której wynika, że stosunek perfuzji krwi w płucach i mózgu może być nową metodą
oceniającą centralizację krążenia.
Cel pracy: Celem badań było określenie współczynnika określającego stosunek przepływów krwi w płucach i mózgu w ciąży o przebiegu prawidłowym i w ciąży wysokiego ryzyka.
Materiał i metody: Przepływ krwi oceniano metodą dopplerowska w proksymalnej części prawej tętnicy płucnej
oraz w tętnicy środkowej mózgu w dwóch grupach pacjentek: u 228 ciężarnych z ciążą pojedynczą o przebiegu
prawidłowym między 22 a 40 tygodniem ciąży oraz u 89 ciężarnych z ciążą wysokiego ryzyka. W oparciu o uzyskane wyniki obliczano stosunek wartości PI w naczyniach płucnych i mózgowych. Uzyskane wyniki odnoszono
do stanu noworodka po porodzie.
Wyniki: W grupie kontrolnej wartości PI tętnicy płucnej są stabilne aż do 30. tygodnia ciąży z następowym nieznacznym wzrostem aż do terminu porodu. Wartości stosunku PI w tętnicy środkowej mózgu do PI prawej tętnicy
płucnej wzrastają między 22. a 28. tygodniem ciąży z następowym spadkiem do terminu porodu. W grupie ciąż
wysokiego ryzyka, nie stwierdzono istotnej zależności między wartościami PI prawej tętnicy płucnej a stanem noworodka po porodzie. W tej grupie ciąż wykładniki centralizacji krążenia wykazywały zależność w odniesieniu do
parametrów charakteryzujących zły stan noworodka po porodzie.
Wnioski: Ocena przepływu krwi w tętnicy środkowej mózgu, w porównaniu z oceną przepływu w tętnicy płucnej,
ma większą wartość predykcyjną w prognozowaniu stanu płodu. Analiza współczynnika – PI mózgu/PI płuc – nie
poprawia tej oceny.
Słowa kluczowe: tĊtnica páucna / tĊtnica ĞrodNoZa my]gu / centrali]acMa NrąĪenia /
/ páyd / Doppler / ciąĪa /
Introduction
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eYaluaWiRQ RI KiJK-risN SreJQaQFies, SarWiFular\ FRPSliFaWeG b\
iQWra-uWeriQe JrRZWK resWriFWiRQ ,8*5 aQG SreJQaQF\ iQGuFeG
K\SerWeQsiRQ 3,+ >1-@
6iJQs RI IeWal braiQ-sSariQJ GuriQJ FKrRQiF K\SR[ia are Zell
esWablisKeG >,@ 6WuGies RQ IeWal sKeeS GuriQJ K\SR[ia KaYe
reYealeG reGisWribuWiRQ RI FirFulaWiRQ IaYRriQJ WKe YiWal RrJaQs
braiQ, KearW aQG aGreQals >@ ,Q e[SeriPeQWal laPb sWuGies, IeWal luQJ blRRG ÀRZ GeFreaseG PRsW RI all RrJaQs sWuGieG GuriQJ
K\SR[ia >@ $WWePSWs KaYe beeQ PaGe WR use WKe DRSSler WeFKQiTue iQ WKe SreGiFWiRQ KuPaQ IeWal FirFulaWiRQ reGisWribuWiRQ GuriQJ FKrRQiF K\SR[ia 5esearFK RQ siJQs RI GeFreaseG ÀRZ WR less
iPSRrWaQW IeWal RrJaQs GuriQJ FeQWralizaWiRQ RI FirFulaWiRQ suFK as
JuW, NiGQe\, liYer, aQG SeriSKeral arWeries KaYe beeQ GisaSSRiQWiQJ
>-11@ +RZeYer, sWuGies RQ IeWal luQJbraiQ FirFulaWiRQ usiQJ GiJiWal aQal\sis RI SRZer DRSSler siJQal iQWeQsiW\ iQ WKe WZR RrJaQs
KaYe suJJesWeG a ParNeG reGuFWiRQ iQ luQJ SerIusiRQ iQ KiJK-risN
SreJQaQFies >2@ %raiQ ÀRZ siJQals Zere iQFreaseG aW WKe saPe
WiPe 7Ke raWiR beWZeeQ luQJbraiQ SerIusiRQ PiJKW WKereIRre JiYe
a QeZ PeWKRG WR SreGiFW IeWal FirFulaWiRQ FeQWralizaWiRQ >2@.
Nr 1/2014
7Ke aiPs RI WKe SreseQW sWuG\ Zere WKereIRre WR RbWaiQ IeWal
riJKW SulPRQar\ arWer\ SulsaWiliW\ iQGe[ 53$ 3, aQG PiGGle Ferebral arWer\ M&$ 3, iQ WKe FRurse RI QRrPal SreJQaQF\ 6eFRQGar\, WR FalFulaWe PiGGle Ferebral arWer\ 3, WR riJKW SulPRQar\
arWer\ 3, raWiR M&$53$-raWiR GuriQJ WKe FRurse RI QRrPal
SreJQaQF\ )iQall\, WR eYaluaWe siJQs RI FirFulaWiRQ reGisWribuWiRQ
iQ WKese Yessels iQ IeWuses aW risN IRr iQWrauWeriQe K\SR[ia
Materials and methods
DRSSler saPSles IrRP SrR[iPal riJKW SulPRQar\ arWer\
blood velocities and middle cerebral artery were recorded in
a cross-sectional study in 22 normal sinJleton SreJnancies at
Jestational aJe 22 to weeNs $ll SreJnancies Kad an uneventIul
course oI SreJnancy, labour and delivery $ll Satients Jave tKeir
inIormed consent and tKe study Srotocol Kas been aSSroved by
tKe +osSital (tKics &ommittee Malmo-6weden *estational aJe
Kad been establisKed in eacK SreJnancy by ultrasound e[amination SerIormed in tKe ¿rst trimester oI SreJnancy
DoSSler samSles Irom tKe Sro[imal riJKt Sulmonary artery
and middle cerebral artery were also recorded in KiJK-risN sinJleton SreJnancies reIerred Ior antenatal blood Àow e[amination
indicated by intra-uterine JrowtK retardation ,8*5 n= and
SreJnancy induced KySertension 3,+ n= 7Ke de¿nition
used as SreJnancy-induced KySertension was values oI blood
© Polskie Towarzystwo Ginekologiczne
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P R A C E O R Y G I N A L N E
poł ożn i ct wo
+MRIOSP4SP
Bręborowicz A, et al. Fetal pulmonary and cerebral artery Doppler velocimetry in normal and high risk pregnancy.
Sressure 1 mm+J, an increase oI systolic blood Sressure
oI mm+J and diastolic blood Sressure oI 1 mm+J above
tKe basic values ([aminations were reSeated in some cases, but
results Irom tKe last e[amination beIore delivery were only correlated to outcome oI SreJnancy Median Jestational aJe at tKe
last e[amination was weeNs ranJe 2- weeNs 7Ke median
interval between tKe e[amination and labour was , days ranJe
- days 7Ke clinicians were only inIormed oI tKe umbilical
8$ and uterine artery 8t$ blood velocimetry, but not oI Ietal
cerebral and Sulmonary blood Àow recordinJ, wKicK were SerIormed at tKe same time as
$cuson ;3 and 6eTuoia ultrasound units 6iemens Medical
&o witK Sulsed, color and Sower DoSSler Sossibilities was used
durinJ tKe study &onventional %-mode sonoJraSKy was used to
visualize tKe Ietal cKest at it¶s transverse, cross-sectional Slane at
tKe level oI tKe Sulmonary artery 7Ke main Sulmonary artery was
located and tKen tKe riJKt Sulmonary artery Must beyond biIurcation oI tKe main Sulmonary artery 12 7Ke blood velocity waveIorm was obtained by SositioninJ tKe DoSSler samSle volume
into Sro[imal Sart oI riJKt Sulmonary artery Must beyond biIurcation oI main Sulmonary artery 7Ke riJKt brancK was cKosen Ior
tKe measurements as tKere is no diIIerence between waveIorms
obtained Irom riJKt and leIt Sulmonary artery >12,1@ &Karacteristic oI riJKt Sulmonary arterial blood velocity waveIorm is
illustrated in )iJure 1
7Ke middle cerebral artery was visualized at tKe level oI
circle oI :illis by tKe use oI color DoSSler 7Ke Sulsed DoSSler
samSle volume was Slaced in tKe middle cerebral artery at near 0
anJles to tKe ultrasound beam and tKe blood velocity waveIorms
were obtained and stored &are was taNen not to SusK on tKe Ietal
Kead, wKile e[amininJ middle cerebral artery as tKat miJKt increase Sressure and, conseTuently reduce cerebral SerIusion >2@
)etal brain sSarinJ eIIect was de¿ned as 3, mean - 26D
8mbilical artery velocimetry was recorded Irom a Iree ÀoatinJ looS oI tKe cord 7Ke blood velocity waveIorm was analysed
Ior 3, and comSared witK normal reIerence values >1@ $ll DoSSler e[aminations were made durinJ absence oI Ietal breatKinJ
movements
Uterine artery blood velocity was located bilaterally by color
Àow maSSinJ in an obliTue scan, witK tKe samSle volume Slaced
in tKe artery Must cranial to tKe aSSarent crossinJ oI tKe e[ternal
iliac blood vessels 7Kree subseTuent blood velocity waveIorms
Ior eacK vessel were analyzed Ior 3, accordinJ to *oslinJ et al,
wKicK is an acNnowledJed measure oI downward vascular imSedance >1@ 7Ke mean oI botK uterine arteries 3, were calculated, 3, e[ceedinJ 120 was deemed abnormal >1@ Middle cerebral artery over riJKt Sulmonary artery 3, ratio M&$53$ 3,
ratio was calculated $ll e[aminations oI normal controls were
SerIormed by one oSerator MD
,n tKe KiJK-risN SreJnancies, tKe DoSSler results were attributed to Serinatal outcome, includinJ Jestational aJe at delivery,
birtKweiJKt, $SJar score at minute oI liIe, umbilical arterial
and venous S+, tKe need Ior oSerative delivery Ior Ietal distress
2D)D, tKe needs Ior admission to neonatal intensive care unit
1,&U, arti¿cial ventilation and Serinatal mortality $ small-IorJestational-aJe 6*$ inIant was de¿ned as birtKweiJKt below
tKe tentK Sercentile Ior corresSondinJ Jestational aJe >1@.
7Ke comSuter soItware 6tatistica version 0 6tat6oIt,
,nc was used Ior statistical analysis 1ormal reIerence cKarts
28
Figure 1. Typical spectrum of blood velocity waveforms of proximal branch right
fetal pulmonary artery in normal pregnancy.
Figure 2. Mean and 95% CI of right proximal pulmonary artery pulsatility index (PI)
in in the second half of pregnancy.
Ior M&$ 3,, 53$ 3, and M&$53$ ratios were constructed by
Solynomial reJression analysis by tKe Tuadratic metKod JivinJ
mean, 2 and Sercentiles cut-oII¶s )isKer¶s e[act test was
used to determine numeric diIIerences between JrouSs witK
normal and abnormal blood Àow velocity 7Ke Mann-:Kitney
non-Sarametric test was used to comSare continuinJ variables in
tKe two JrouSs
Results
5iJKt Sulmonary artery 3, in tKe normal controls remained
stable until 0 weeNs oI Jestation witK sliJKt increase tKereaIter
until term )iJure 2 ,n tKe course oI normal SreJnancy tKe middle cerebral artery curve is Tuite similar to tKe curve Sresented by
Mari and Deter >1@ )iJure 7Ke middle cerebral artery to riJKt Sulmonary artery M&$
53$ 3, ratio increased between 22 and 2 weeNs oI Jestation
witK tKe raSid Iall towards term )iJure ,n tKe KiJK-risN SreJnancy JrouS, tKe median Jestational aJe
at delivery was weeNs ranJe 2-1 weeNs
© Polskie Towarzystwo Ginekologiczne
Nr 1/2014
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O R Y G I N A L N E
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Bręborowicz A, et al. Fetal pulmonary and cerebral artery Doppler velocimetry in normal and high risk pregnancy.
,n tKe KiJK-risN SreJnancies, 0 Kad a normal Sro[imal riJKt Sulmonary artery 3, 7Kere were no siJni¿cant diIIerences in Serinatal outcome between cases witK normal and
abnormal Sulmonary artery 3, 6iJns oI brain-sSarinJ in M&$
were Iound in Ietuses and was KiJKly correlated in all
adverse outcome Sarameters e[ceSt 6*$ newborns 7Ke JrouS oI
KiJK-risN SreJnancies consists oI 1 Ietuses witK abnormal
M&$53$ 3, ratio 6iJni¿cance oI diIIerences was Iound in all
Sarameters studied e[ceSt 6*$ newborns, ventilation in 1,&U
and 2D)D
Discussion
Figure 3. Mean and 95%CI of middle cerebral artery pulsatility index (PI) in in the
second half of pregnancy.
Figure 4. Mean and 95%CI of middle cerebral artery pulsatility index (PI) over right
pulmonary artery PI ratio (MCA/RPA) in the second half of pregnancy.
7Ke mean birtKweiJKt oI inIants was 10“ J and 1 newborns were small-Ior-Jestational aJe at birtK 7Ke
needs Ior 2D)D were in 2 cases and neonates were admitted
to 1,&U, wKere oI tKem were ventilated $SJar score at min was Iound in 1 $rterial S+ 1 and venous S+ 20 was
Iound in 2 and 2 cases, resSectively 7Kere were seven Serinatal
deatKs ± all aIter delivery due to severe ,U*5 and Srematurity
2 weeNs oI Jestational aJe ± 10J 2 weeNs oI Jestational
aJe ± 20J 2 weeNs oI Jestational aJe ± 0J 2 weeNs oI
Jestational aJe ± 0J 2 weeNs oI Jestational aJe ± 0J 2
weeNs ± 0J 2 weeNs ± 0J
Nr 1/2014
7Ke results demonstrate a cKanJe in Ietal 53$ and M&$
blood Àow witK advancinJ Jestation in second KalI oI SreJnancy
M&$ 53$ 3, ratio was also demonstrated Irom 22nd to 0th week
oI SreJnancy 7he analysis oI blood Àow in hiJh-risk SreJnancies
showed that riJht Sulmonary artery 3, seems to be a Soor marker
in SredictinJ Serinatal outcome 7here were no diIIerences in
Serinatal outcome between Ietus with normal and abnormal riJht
Sulmonary artery 3, +owever, an abnormal M&$53$ ratio was
related to adverse outcome, but this was mainly due to chanJes
in M&$ 3, 7his study revealed that middle cerebral artery 3,
better corresSond with chanJes in Ietal redistribution and adverse
outcome oI SreJnancy than does the 53$
$lthouJh 1 Ietuses maniIested abnormal values oI M&$
53$-ratio, M&$-3, seemed to be a better Sredictor oI adverse
Serinatal outcome than was M&$53$-3,-ratio )urthermore,
the JrouS oI Ietuses with abnormal riJht Sulmonary artery 3,
consisted oI 0 Ietuses ± only , oI the hiJh-risk SreJnancy
JrouS 7his suJJests that riJht Sulmonary artery blood Àow miJht
chanJe durinJ Ietal circulation redistribution, but this reaction is
Srobably not constant durinJ this Seriod and miJht occur in the
beJinninJ oI this Srocess 5esults by -ensen et al suJJests that
lunJ SerIusion miJht be imSroved aIter reSeated hySo[ic insult
>1@
5asanen et al described decrease oI Sulsatility inde[ 3,
oI Sro[imal Sulmonary artery with advanced Jestational aJe until th week oI Jestation >12@ 7he conÀictinJ results between
the Sresent study on normal controls and the Srevious study by
5asanen et al may be e[Slained by the diIIerence in number oI
investiJated Satients, as their SoSulation JrouS consisted oI only
100 Satients >12@
5en-,nJ /ianJ et al in their study analyzed diIIerences between multiJate sSectral DoSSler scanninJ with the Sower DoSSler imaJinJ oStion and traditional sSectral DoSSler ultrasonoJraShy with color Àow maSSinJ >1@ 7heir study revealed a siJni¿cant diIIerence between main Sulmonary artery and SeriSheral
blood Àow 7his may e[Slain Srevious results in studies on Ietal
brain lunJ circulation usinJ diJital analysis oI Sower DoSSler
siJnal intensity, where a marked reduction in lunJ SerIusion was
seen in hiJh-risk SreJnancies 7he 3ower DoSSler miJht thus reÀect tissue SerIusion, while sSectral DoSSler reÀects vascular imSedance in the vessel 7his miJht e[Slain the conÀictinJ results
oI Sresent study and a Srevious results >2@
6tudies on animal and the human Ietus have shown that Ietal
cardiac outSut is redistributed durinJ hySo[ia, IavorinJ vital orJans such as the brain, heart and adrenals >@ %y reducinJ blood
Àow to less imSortant orJans the need Ior o[yJen and nutrients
is reduced and the Ietus is able to maintain o[yJen and blood
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Bręborowicz A, et al. Fetal pulmonary and cerebral artery Doppler velocimetry in normal and high risk pregnancy.
Jas status within normal limits %lood S+ may remain stable due
this Shenomenon 7he centralization oI Ietal circulation results in
reduced Àow in the kidneys and Jut, which may cause oliJohydramnios and necrotizinJ enterocolitis in the newborn &irculation redistribution miJht also lead to asymmetrical Jrowth oI the
Ietal body
6tudies Iocused on Ietal suSerior mesenteric and heSatic
arteries revealed that siJns oI redistribution in the mesenteric
artery miJht be a late siJn oI Ietal comSromise >@ The vascular
sSarinJ oI the Ietal liver can be seen at an early staJe oI Ietal
comSromise This sSarinJ eIIect seems to disaSSear in severely
comSromised Ietuses1 The velocimetry oI sSlenic artery and 3,
values in the course oI hiJh-risk remained within normal values
>20@ $rudini et al revealed in their studies on the renal artery,
that blood Àow in this vessel is decreased durinJ lonJ term
Ietal hySo[ia >21@ 6tiJter et al studied inÀuence oI chanJes
in Ietal renal artery on Ietal condition in the Jrowth-restricted
Sreterm Ietus >22@ They revealed that redistribution is reÀected
by chanJes oI Seak-systolic velocities rather than by chanJes
in Sulsatility inde[ 6Sectrum oI both the renal and Sulmonary
blood velocity has low Àow velocities in diastole &hanJes durinJ
reduction miJht be diI¿cult to interSret by DoSSler, esSecially in
the severely aIIected Ietus where reversal oI venous Àow durinJ
atrial contraction miJht be suSerimSosed in the diastolic Àow
Sattern
The evaluation oI Slacental and Ietal liver, adrenals, kidney,
and lunJ blood Àow by Sower-DoSSler ultrasound has imSroved
our knowledJe on Ietal circulation ,n normal SreJnancy, the
Sower-DoSSler comSuter analyzed siJnal intensity seems to increase in all orJans with Jestation uS to weeks, aIter which
a decline in intensity is noted >11@ The chanJe in the other orJans
miJht be e[Slained by centralization oI Ietal circulation secondary to IailinJ Slacental Iunction ,n hiJh-risk SreJnancies the decrease in orJan blood Àow is even more Sronounced, suJJestinJ
Iurther develoSment oI Ietal circulatory centralization >@ )etal
cerebral Sower-DoSSler siJnal intensity and the brainlunJ-ratio
increases towards the end oI normal SreJnancy The data Irom the
Srevious study shows that Sower DoSSler reSresents centralization oI Ietal circulation durinJ chronic hySo[ia by evaluation oI
Ietal orJan tissue SerIusion, rather than vascular imSedance
Conclusion
The main conclusion oI this study is that velocimetry oI the
middle cerebral artery is better than velocimetry oI riJht Sulmonary artery in SredictinJ outcome in hiJh-risk SreJnancy M&$
53$ 3, ratio was oI limited value in SredictinJ redistribution oI
Ietal circulation in hiJh-risk SreJnancies
Acknowledgements:
The medical faculty, University of Lund, research funds at the University
hospital in Malmö and Region Skåne supported the study.
Oświadczenie autorów
1. Andrzej Bręborowicz – autor koncepcji i założeń pracy, zebranie materiału,
przygotowanie manuskryptu, analiza wyników, zebranie piśmiennictwa.
2. Mariusz Dubiel – zebranie materiału, analiza statystyczna wyników,
przygotowanie manuskryptu.
3. Marek Pietryga – współautor tekstu pracy, współautor protokołu i aktualizacja literatury.
30
4.
5.
Grzegorz H. Bręborowicz – autor założeń pracy, analizy i interpretacji
wyników, przygotowanie, korekta i akceptacja ostatecznego kształtu pracy
– autor zgłaszający i odpowiedzialny za manuskrypt.
Saemundur Gudmundsson – udział w przygotowaniu koncepcji badań,
korekta oraz ostateczne zatwierdzenie manuskryptu.
Źródło finansowania:
Praca nie była finansowana przez żadną instytucję naukowo-badawczą,
stowarzyszenie ani inny podmiot, autorzy nie otrzymali żadnego grantu.
Konflikt interesów:
Autorzy nie zgłaszają konfliktu interesów oraz nie otrzymali żadnego
wynagrodzenia związanego z powstawaniem pracy.
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