Zusammenfassung
Hintergrund
Die Bilder einer systolischen Schulter im Dopplermuster der A. cerebri media (ACM) des Feten oder der A. uterina (A. ut.) der Mutter bei schwerer Präeklampsie (PE) sind sicher vielen Untersuchern begegnet. Bisher scheint es keine schlüssige Erklärung für diese Veränderungen zu geben.
Fragestellung
Hämodynamische Untersuchungen belegen, dass Vasokonstriktion und PW(Pulswellen)-Reflexion im systemischen Kreislauf mit dem Auftreten einer systolischen Schulter in systemischen und v. a. in zerebralen Gefäßen einhergehen. Damit stellt sich die Frage, ob diese Dopplerveränderungen bei Mutter und (ungeborenem) Kind als Folge erhöhter peripherer Vasokonstriktion interpretiert werden können.
Material und Methode
In der Hämodynamik ist das Modell der PW-Ausbreitung und -Reflexion gut etabliert. Bei schwerer PE wird damit die PW-Reflexionszeit Tr (= Transitzeit bis zur Reflexion und zurück) ermittelt und mit dem Intervall bis zur systolischen Schulter in der A. ut. verglichen. Übertragen auf den fetalen Kreislauf werden mithilfe der PW-Geschwindigkeit in der Aorta und der funktionellen Reflexionsdistanz die PW-Reflexionszeit beim Feten ermittelt und mit dem Intervall bis zur ACM-Schulter verglichen.
Ergebnisse
Die Berechnung der jeweiligen PW-Reflexionszeit Tr ergab eine gute Übereinstimmung mit den beobachteten Zeitintervallen ∆t bis zur systolischen Schulter im Dopplerbefund. Die Gabe von Vasodilatatoren führte zur Abnahme bzw. zum Verschwinden der systolischen Schulter.
Diskussion
Die Ergebnisse belegen die Validität des PW-Modells, d. h.: Die systolische Schulter im Dopplerbefund der A. ut. und der ACM kann als Zeichen der PW-Reflexion infolge peripherer Vasokonstriktion interpretiert werden. Dies ist prospektiv von Nutzen beim Monitoring der progredienten PE und in der ACM als Indikator für fetale Stressreaktionen.
Abstract
Background
The Doppler pattern of a systolic shoulder in the middle cerebral artery (MCA) of the fetus or in the uterine artery (UtA) of a mother with severe pre-eclampsia (PE) have certainly been encountered by many investigators; however, so far there seems to be no conclusive explanation for these changes.
Objective
Hemodynamic studies in the arterial system confirmed that vasoconstriction and pulse wave (PW) reflection in the systemic circulation are associated with the appearance of a systolic shoulder in systemic and especially in cerebral arteries. This raises the question whether these Doppler changes in mother and (unborn) child may be interpreted as a consequence of increased peripheral vasoconstriction.
Material and methods
In hemodynamics, the model of PW propagation and reflection is well-established. Accordingly, in severe PE the PW reflection time Tr (= transit time to reflection and return) is determined and compared with the interval to the systolic shoulder onset in the UtA. Applied to the fetal circulation, the PW reflection time is calculated using PW velocity in the fetal aorta and functional distance to reflection and compared with the interval to MCA shoulder onset.
Results
The model calculation of the respective PW reflection times Tr showed good agreement with the observed time intervals ∆t to systolic shoulder onset in the Doppler waveform for both the mother and the fetus. Furthermore, a decrease or even disappearance of the systolic shoulder was observed after administration of drugs with vasodilating effects.
Conclusion
The model results substantiate the validity of the PW model for the interpretation of this particular Doppler pattern. The systolic shoulder in the Doppler waveform of the maternal UtA and the fetal MCA can be interpreted as a sign of PW reflection due to peripheral vasoconstriction. Regarding the UtA this interpretation of the systolic shoulder may prove useful in monitoring progressive PE and in the MCA may indicate fetal stress response.
Literatur
Abbasi N, Johnson JA, Ryan G (2017) Fetal anemia. Ultrasound Obstet Gynecol 50:145–153
Adamson SL, Whiteley KJ, Langille BL (1992) Pulsatile pressure-flow relations and pulse-wave propagation in the umbilical circulation of fetal sheep. Circ Res 70:761–772
Amit A, Thaler I, Paz Y, Itskovitz-Eldor J (1998) The effect of a nitric oxide donor on Doppler flow velocity waveforms in the uterine artery during the first trimester of pregnancy. Ultrasound Obstet Gynecol 11:94–98
Avni B, Frenkel G, Shahar L et al (2010) Aortic stiffness in normal and hypertensive pregnancy. Blood Press 19:11–15
Bamfo JEAK, Kametas N, Nicolaides KH et al (2007) Reference ranges for tissue Doppler measures of maternal systolic and diastolic left ventricular function. Ultrasound Obstet Gynecol 29:414–420
Berger DS, Li JK, Laskey WK, Noordergraaf A et al (1993) Repeated reflection of waves in the systemic arterial system. Am J Physiol 264:H269–H281
Bhide A, Johnson J, Rasanen J et al (2019) Fetal heart rate variability with hypoxemia in an instrumented sheep model. Ultrasound Obstet Gynecol 54:786–790
Cheung YF, Taylor MJ, Fisk NM et al (2000) Fetal origins of reduced arterial distensibility in the donor twin in twin-twin transfusion syndrome. Lancet 355(9210):1157–1158
Cobelli C, Carson E (2008) Introduction to modeling in physiology and medicine. Academic Press, Amsterdam
Cruz-Martinez R, Figueras F (2009) The role of Doppler and placental screening. Best Pract Res Clin Obstet Gynaecol 23:845–855
Diehl W, Hecher K (2013) Mehrlingsschwangerschaft. In: Gembruch U, Hecher K, Steiner H (Hrsg) Ultraschalldiagnostik in Geburtshilfe und Gynäkologie. Springer, Heidelberg, S 495–518 (Abb. 20.30a)
Easterling TR (2014) Pharmacological management of hypertension in pregnancy. Semin Perinatol 38:487–495
Espinoza J, Espinoza AF (2011) Pre-eclampsia: a maternal manifestation of a fetal adaptive response? Ultrasound Obstet Gynecol 38:367–370
Fan FC, Chen RY, Schuessler GB et al (1980) Effects of hematocrit variations on regional hemodynamics and oxygen transport in the dog. Am J Physiol 238:H545–H552
Figueras F, Gardosi J (2011) Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 204:288–300
Franz MB, Burgmann M, Neubauer A et al (2013) Augmentation index and pulse wave velocity in normotensive and pre-eclamptic pregnancies. Acta Obstet Gynecol Scand 92:960–966
Fumia FD, Edelstone DI, Holzman IR (1984) Blood flow and oxygen delivery to fetal organs as functions of fetal hematocrit. Am J Obstet Gynecol 150:274–282
Gardiner HM (2008) Intrauterine programming of the cardiovascular system. Ultrasound Obstet Gynecol 32:481–484
Gardiner HM, Taylor MJ, Karatza A et al (2003) Twin-twin transfusion syndrome: the influence of intrauterine laser photocoagulation on arterial distensibility in childhood. Circulation 107:1906–1911
Gómez-Arriaga PI, Herraiz I, López-Jiménez EA et al (2014) Uterine artery Doppler and sFlt-1/PlGF ratio: prognostic value in early-onset pre-eclampsia. Ultrasound Obstet Gynecol 43:525–532
Gonser M (2019) Hemodynamic relationship between ophthalmic artery and uterine artery in pre-eclampsia: pulse wave reflection and transmission might provide the missing link. Ultrasound Obstet Gynecol 53:135–136
Gonser M (2020) Bedeutung der A. ophthalmica in der zukünftigen Funktionsdiagnostik bei Präeklampsie. Gynäkologe 53:486–488
Gonser M, Klee A, Seidel V (2019) Preeclampsia with doppler signs of increased pulse wave reflection in uterine and ophthalmic artery: association with extreme levels of angiogenic markers of placental dysfunction. Z Geburtshilfe Neonatol 223(S 01):E23
Gonser M, Pahlevan NM, Gharib M (2020) Optimization criterion for pulsatile timing: observation in the human fetus. Ultrasound Obstet Gynecol 56(S1):197–198
Gonser M, Tavares de Sousa M, Klee A, Hecher K (2018) A systolic shoulder in fetal middle cerebral artery Doppler waveforms may indicate fetal pulse wave reflection and transmission to cerebral circulation—a contribution to fetal circulatory physiology. Ultraschall Med 39(S 01):S27
Gonser M, Tavares de Sousa M, Klee A, Hecher K (2018) Second systolic peak in middle cerebral artery Doppler of fetuses with severe anemia: an explanatory model based on fetal pulse wave reflection. Ultrasound Obstet Gynecol 52:555
Gonser M, Wessler K, Klee A (2017) Systolic notch in severe preeclampsie—a Doppler marker of maternal hemodynamic dysfunction? Pregnancy Hypertens 9:25
Hashimoto J, Westerhof BE, Ito A (2018) Carotid flow augmentation, arterial aging, and cerebral white matter hyperintensities. Comparison with pressure augmentation. Arterioscler Thromb Vasc Biol 38(12):2843–2853
Heffernan KS, Lefferts WK, Augustine JA (2013) Hemodynamic correlates of late systolic flow velocity augmentation in the carotid artery. Int J Hypertens 2013:920605
Hill AA, Surat DR, Cobbold RS et al (1995) A wave transmission model of the umbilicoplacental circulation based on hemodynamic measurements in sheep. Am J Physiol 269:R1267–R1278
Kaihura C, Savvidou MD, Anderson JM et al (2009) Maternal arterial stiffness in pregnancies affected by preeclampsia. Am J Physiol Heart Circ Physiol 297:H759–H764
Khalil A, Garcia-Mandujano R, Maiz N et al (2014) Longitudinal changes in maternal hemodynamics in a population at risk for pre-eclampsia. Ultrasound Obstet Gynecol 44:197–204
Langille BL, Adamson SL (1992) Thoracic aortic pressure-flow relationships and vascular impedance in fetal sheep. Am J Physiol 263:H824–H832
Liang F, Oshima M, Huang H, Liu H, Takagi S (2015) Numerical study of cerebroarterial Hemodynamic changes following carotid artery operation: a comparison between multiscale modeling and stand-alone three-dimensional modeling. J Biomech Eng 137(10):101011
Luzi G, Caserta G, Iammarino G (1999) Nitric oxide donors in pregnancy: fetomaternal hemodynamic effects induced in mild pre-eclampsia and threatened preterm labor. Ultrasound Obstet Gynecol 14:101–109
Macedo ML, Luminoso D, Savvidou MD et al (2008) Maternal wave reflections and arterial stiffness in normal pregnancy as assessed by applanation tonometry. Hypertension 51:1047–1051
Mahmud A (2007) Reducing arterial stiffness and wave reflection—quest for the holy grail? Artery Res 1:13–19
Mari G, Moise KJ Jr, Deter RL et al (1990) Flow velocity waveforms of the umbilical and cerebral arteries before and after intravascular transfusion. Obstet Gynecol 75:584–589
Maršál K, Vetter K (2020) Konsequenzen aus intrauterin erkannter plazentarer Versorgungsstörung. Gynäkologe 53(7):444–454
Martin H, Hu J, Gennser G et al (2000) Impaired endothelial function and increased carotid stiffness in 9‑year-old children with low birthweight. Circulation 102:2739–2744
Martyn CN, Barker DJ, Jespersen S et al (1995) Growth in utero, adult blood pressure, and arterial compliance. Br Heart J 73:116–121
Matias DS, Costa RF, Matias B et al (2012) Ophthalmic artery doppler velocimetric values in pregnant women at risk for preeclampsia. J Ultrasound Med 31:1659–1664
McLaughlin K, Scholten RR, Floras JS et al (2018) Should maternal hemodynamics guide antihypertensive therapy in preeclampsia? Hypertens 71:550–556
Melchiorre K, Sharma R, Thilaganathan B (2014) Cardiovascular implications in preeclampsia: an overview. Circulation 133:703–714
Mills CJ, Gabe IT, Gault JH, Mason DT, Ross J Jr, Braunwald E, Shillingford JP (1970) Pressure-flow relationships and vascular impedance in man. Cardiovasc Res 4:405–417
Mynard JP, Kowalski R, Cheung MMH (2017) Beyond the aorta: partial transmission of reflected waves from aortic coarctation into supra-aortic branches modulates cerebral hemodynamics and left ventricular load. Biomech Model Mechanobiol 16:635–650
Nakatsuka M, Takata M, Tada K et al (2002) Effect of a nitric oxide donor on the ophthalmic artery flow velocity waveform in preeclamptic women. J Ultrasound Med 21:309–313
Nichols WW, O’Rourke MF (1990) McDonald’s blood flow in arteries: theoretical, experimental and clinical principles, 3. Aufl. Arnold, London
O’Rourke MF, Adji A, Michel E, Safar ME (2018) Structure and function of systemic arteries: reflections on the arterial pulse. Am J Hypertens 31:934–940
Pahlevan NM, Gharib M (2014) A wave dynamics criterion for optimization of mammalian cardiovascular system. J Biomech 47:1727–1732
Pahlevan NM, Mazandarani SP (2020) Estimation of wave condition number from pressure waveform alone and its changes with advancing age in healthy women and men. Front Physiol 11:313
Polat I, Gedikbasi A, Kiyak H et al (2015) Double notches: association of uterine artery notch forms with pregnancy outcome and severity of preeclampsia. Hypertens Pregnancy 34:90–101
Pozniak MA, Allan PL (2013) Clinical doppler ultrasound, 3. Aufl. Churchill Livingstone, Edinburgh
Rodriguez C, Chi YY, Chiu KH et al (2018) Wave reflections and global arterial compliance during normal human pregnancy. Physiol Rep 6:e13947
Rönnback M, Lampinen K, Groop PH et al (2005) Pulse wave reflection in currently and previously preeclamptic women. Hypertens Pregnancy 24:171–180
Savvidou MD, Kaihura C, Anderson JM et al (2011) Maternal arterial stiffness in women who subsequently develop pre-eclampsia. Plos One 6:e18703
Schoofs K, Grittner U, Engels T et al (2014) The importance of repeated measurements of the sFlt-1/PlGF ratio for the prediction of preeclampsia and intrauterine growth restriction. J Perinat Med 42:61–68
Shah DA, Khalil RA (2015) Bioactive factors in uteroplacental and systemic circulation link placental ischemia to generalized vascular dysfunction in hypertensive pregnancy and preeclampsia. Biochem Pharmacol 95:211–226
Sohn C, Kagan KO, Fluhr H, Vetter K (Hrsg) (2018) Kursbuch Dopplersonographie in Gynäkologie und Geburtshilfe. Thieme, Stuttgart
Struijk PC, Migchels H, Mathews JV et al (2013) Fetal aortic distensibility, compliance and pulse pressure assessment during the second half of pregnancy. Ultrasound Med Biol 39:1966–1975
Szpinda M (2008) Length growth of the various aortic segments in human foetuses. Folia Morphol 67:245–250
Szpinda M, Szpinda A, Woźniak A et al (2012) The normal growth of the common iliac arteries in human fetuses—an anatomical, digital and statistical study. Med Sci Monit 18:BR109–BR116
Takata M, Nakatsuka M, Kudo T (2002) Differential blood flow in uterine, ophthalmic, and brachial arteries of preeclamptic women. Obstet Gynecol 100:931–939
Thaler I, Amit A, Kamil D, Itskovitz-Eldor J (1999) The effect of isosorbide dinitrate on placental blood flow and maternal blood pressure in women with pregnancy induced hypertension. Am J Hypertens 12:341–347
Thaler I, Weiner Z, Itskovitz J (1992) Systolic or diastolic notch in uterine artery blood flow velocity waveforms in hypertensive pregnant patients: relationship to outcome. Obstet Gynecoi 80:277–282
Thilaganathan B (2018) Pre-eclampsia and the cardiovascular-placental axis. Ultrasound Obstet Gynecol 51:714–717
Verlohren S, Perschel FH, Thilaganathan B et al (2017) Angiogenic markers and cardiovascular indices in the prediction of hypertensive disorders of pregnancy. Hypertension 69:1192–1197
Vonzun L, Ochsenbein-Koelble N, Zimmermann R, Gonser M (2019) Second systolic peak in middle cerebral artery Doppler: a sign of hypoxemia induced fetal pulse wave reflection after intrauterine transfusion. Ultrasound Obstet Gynecol 54:142–143
Danksagung
für Geduld, Langmut und Unterstützung auf vielfältige Weise, an: Nicole Ochsenbein-Kölble, Ladina Vonzun, Manuela Tavares de Sousa, Kurt Hecher, Roland Zimmermann, Torvid Kiserud und Klaus Vetter, als unermüdlicher Mentor.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Interessenkonflikt
M. Gonser gibt an, dass kein Interessenkonflikt besteht.
Für diesen Beitrag wurden keine Untersuchungen an Patienten vorgenommen. Es handelt sich ausschließlich um retrospektive Auswertungen von Befunden und Daten abgeschlossener Behandlungen gemäß den Empfehlungen der jeweiligen Ethik-Kommissionen und Ärztekammern.
Additional information
Redaktion
R. Zimmermann, Zürich
K. Vetter, Berlin
Rights and permissions
About this article
Cite this article
Gonser, M. Die etwas andere Dopplersonographie – Zeichen der Pulswellenreflexion bei Mutter und (ungeborenem) Kind. Gynäkologe 53, 821–830 (2020). https://doi.org/10.1007/s00129-020-04712-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00129-020-04712-1