Abstract
The ductus venosus is a vascular shunt situated within the fetal liver parenchyma, connecting the umbilical vein to the inferior vena cava. This vessel acts as a bypass of the liver microcirculation and plays a critical role in the fetal circulation. The ductus venosus allows oxygenated and nutrient-rich venous blood to flow from the placenta to the myocardium and brain. Increased impedance to flow in the fetal ductus venosus is associated with fetal aneuploidies, cardiac defects and other adverse pregnancy outcomes. This review serves to improve our understanding of the mechanisms that regulate the blood flow redistribution between the fetal liver circulation and fetal heart and the clinical significance of the ductus venosus waveform as generated by pressure-volume changes in the fetal heart.
Keywords: Ductus venosus, fetal venous circulation, ductus venosus shunting, ultrasound, doppler velocimetry, heart.
Graphical Abstract
[1]
Kiserud T, Eik-Nes SH, Blaas HG, Hellevik LR. Ultrasonographic velocimetry of the fetal ductus venosus. Lancet 1991; 338(8780): 1412-4.
[3]
Tchirikov M, Schröder HJ, Hecher K. Ductus venosus shunting in the fetal venous circulation: Regulatory mechanisms, diagnostic methods and medical importance. Ultrasound Obstet Gynecol 2006; 27(4): 452-61.
[5]
Tchirikov M, Schlabritz-Loutsevitch NE, Hubbard GB, Nathanielsz PW, Beindorff N, Schroder HJ. Ductus venosus shunting in marmoset and baboon fetuses. Ultrasound Obstet Gynecol 2005; 26: 252-7.
[6]
Matias A, Huggon I, Areias JC, Montenegro N, Nicolaides KH. Cardiac defects in chromosomally normal fetuses with abnormal ductus venosus blood flow at 10-14 weeks. Ultrasound Obstet Gynecol 1999; 14(5): 307-10.
[7]
Matias A, Montenegro N, Areias JC, Leite LP. Haemodynamic evaluation of the first trimester fetus with special emphasis on venous return. Hum Reprod Update 2000; 6(2): 177-89.
[8]
Matias A, Montenegro N. Ductus venosus blood flow in chromosomally abnormal fetuses at 11 to 14 weeks of gestation. Semin Perinatol 2001; 25(1): 32-7.
[9]
Matias A, Montenegro N, Loureiro T, et al. Screening for twin-twin transfusion syndrome at 11-14 weeks of pregnancy: The key role of ductus venosus blood flow assessment. Ultrasound Obstet Gynecol 2010; 35(2): 142-8.
[10]
Byrd N, Grabel L. Hedgehog signaling in murine vasculogenesis and angiogenesis. Trends Cardiovasc Med 2004; 14: 308-13.
[11]
Eric D. Endean, Bruce E. Maley. Rutherford's Vascular Surgery / [edited by] Jack L. Cronenwett, K. Wayne Johnston, by Saunders, an imprint of Elsevier Inc., Eighth Edition, 2014, Chapter 2, 15-33.
[12]
Zhan W, Yatskievych TA, Baker RK, Antin PB. Regulation of Hex gene expression and initial stages of avian hepatogenesis by Bmp and Fgf signaling. Dev Biol 2004; 268: 312-26.
[13]
Red-Horse K, Crawford Y, Shojaei F, Ferrara N. Endothelium microenvironment interactions in the developing embryo and in the adult. Dev Cell 2007; 12(2): 181-94.
[14]
Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007; 8(6): 464-78.
[15]
Tchirikov M, Rybakowski C, Huneke B. Schr oder HJ. Blood flow through the ductus venosus in singleton and multifetal pregnancies and in fetuses with I ntrauterine growth retardation. Am J Obstet Gynecol 1998; 178: 943-9.
[16]
Bellotti M, Pennati G, De Gasperi C, Bozzo M, Battaglia FC, Ferrazzi E. Simultaneous measurements of umbilical venous, fetal hepatic, and ductus venosus blood flow in growth-restricted human fetuses. Am J Obstet Gynecol 2004; 190: 1347-58.
[17]
Power GG, Longo LD. Fetal circulation times and their implications for tissue oxygenation. Gynecol Invest 1975; 6: 342-55.
[18]
Edelstone DI, Rudolph AM, Heymann MA. Effects of hypoxemia and decreasing umbilical flow liver and ductus venosus blood flows in fetal lambs. Am J Physiol 1980; 238: H656-63.
[19]
Reuss ML, Rudolph AM. Distribution and recirculation of umbilical and systemic venous blood flow in fetal lambs during hypoxia. J Dev Physiol 1980; 2: 71-84.
[20]
Itskovitz J, Goetzman BW, Rudolph AM. Effects of hemorrhage on umbilical venous return and oxygen delivery in fetal lambs. Am J Physiol 1982; 242: H543-8.
[21]
Itskovitz J, LaGamma EF, Rudolph AM. Effects of cord compression on fetal blood flow distribution and O2 delivery. Am J Physiol 1987; 252: H100-9.
[22]
Paulick RP, Meyers RL, Rudolph CD, Rudolph AM. Venous responses to hypoxemia in the fetal lamb. J Dev Physiol 1990; 14: 81-8.
[23]
Paulick RP, Meyers RL, Rudolph CD, Rudolph AM. Umbilical and hepatic venous responses to circulating vasoconstrictive hormones in fetal lamb. Am J Physiol 1991; 260: H1205-13.
[24]
Jensen A, Roman C, Rudolph AM. Effects of reducing uterine blood flow on fetal blood flow distribution and oxygen delivery. J Dev Physiol 1991; 15: 309-23.
[25]
Kiserud T, Ozaki T, Nishina H, Rodeck C, Hanson MA. Effect of NO, phenylephrine, and hypoxemia on ductus venosus diameter in fetal sheep. Am J Physiol 2000; 279: H1166-71.
[26]
Tchirikov M, Hecher K, Deprest J, Zikulnig L, Devlieger R, Schr̈oder HJ. Doppler ultrasound measurements in the central circulation of anesthetized fetal sheep during obstruction of umbilical – placental blood flow. Ultrasound Obstet Gynecol 2001; 18: 656-61.
[27]
Behrman RE, Lees MH, Peterson EN, De Lannoy CW, Seeds AE. Distribution of the circulation in the normal and asphyxiated fetal primate. Am J Obstet Gynecol 1970; 108: 956-69.
[28]
Paton JB, Fisher DE, DeLannoy CW, Behrman RE. Umbilical blood flow, cardiac output, and organ blood flow in the immature baboon fetus. Am J Obstet Gynecol 1973; 117: 560-6.
[29]
Rudolph AM, Heymann MA, Teramo KAW, Barrett CT, Raiha NCR. Studies on the circulations of the previable human fetus. Pediatr Res 1971; 5: 452-65.
[30]
Kiserud T, Rasmussen S, Skulstad S. Blood flow and the degree of shunting through the ductus venosus in the human fetus. Am J Obstet Gynecol 2000; 182: 147-53.
[31]
Bellotti M, Pennati G. De Gasper iC, Battaglia FC, Ferrazzi E. Role of ductus venosus in distribution of umbilical blood flow in human fetuses during second half of pregnancy. Am J Physiol Heart Circ Physiol 2000; 279: H1256-63.
[32]
Haugen G, Kiserud T, Godfrey K, Crozier S, Hanson M. Portal and umbilical venous blood supply to the liver in the human fetus near term. Ultrasound Obstet Gynecol 2004; 24: 599-605.
[33]
Tchirikov M, Eisermann K, Rybakowski C, Schr̈oder HJ. Doppler ultrasound evaluation of ductus venosus blood flow during acute hypoxemia in fetal lambs. Ultrasound Obstet Gynecol 1998; 11: 426-31.
[34]
Maiz N, Kagan KO, Milovanovic Z, Celik E, Nicolaides KH. Learning curve for Doppler assessment of ductus venosus flow at 11 + 0 to 13 + 6 weeks’ gestation. Ultrasound Obstet Gynecol 2008; 31(5): 503-6.
[35]
Gürses C. How to get ductus venosus flow velocity waveforms between 11 and 14 weeks: Candle flame and falling drop signs. Med Ultrason 2016; 18(4): 528-9.
[36]
Wiechec M, Nocun A, Matyszkiewicz A, Wiercinska E, Latała E. First trimester severe ductus venosus flow abnormalities in isolation or combination with other markers of aneuploidy and fetal anomalies. J Perinat Med 2016; 44(2): 201-9.
[37]
Kagan KO, Wright D, Nicolaides KH. First-trimester contingent screening for trisomies 21, 18 and 13 by fetal nuchal translucency and ductus venosus flow and maternal blood cell-free DNA testing. Ultrasound Obstet Gynecol 2015; 45(1): 42-7.
[38]
Togrul C, Ozaksit GM, Seckin KD, Baser E, Karsli MF, Gungor T. Is there a role for fetal ductus venosus and hepatic artery Doppler in screening for fetal aneuploidy in the first trimester? J Matern Fetal Neonatal Med 2015; 28(14): 1716-9.
[39]
Florjański J, Fuchs T, Zimmer M, Homola W, Pomorski M, Blok D. The role of ductus venosus Doppler flow in the diagnosis of chromosomal abnormalities during the first trimester of pregnancy. Adv Clin Exp Med 2013; 22(3): 395-401.
[40]
Sabria J, Comas C, Barceló-Vidal C, et al. Cumulative sum plots and retrospective parameters in first-trimester ductus venosus quality assurance. Prenat Diagn 2013; 33(4): 384-90.
[41]
Karakoç G, Yavuz A, Eriş Yalçın S, Akkurt MÖ, Danışman N. The significance of reverse flow in ductus venosus between sixteen and twenty weeks’ gestation. Turk J Obstet Gynecol 2017; 14(1): 23-7.
[42]
Suksai M, Suwanrath C, Kor-Anantakul O, Geater A. Time interval measurements of the ductus venosus during the early second trimester of pregnancy: Reference ranges and clinical application. J Ultrasound Med 2018; 37(3): 745-53.
[43]
Pokharel P, Ansari MA. Fetal ductus venosus pulsatility index and diameter during second and third trimester of gestation. J Nepal Med Assoc 2017; 56(205): 124-31.
[44]
İlhan G, İyibozkurt AC, Kalelioğlu Hİ, et al. Effects of fetal cardiac anomalies on ductus venosus and aortic isthmus doppler profiles. Arch Gynecol Obstet 2016; 293(2): 345-50.
[45]
Martins WP, Kiserud T. How to record ductus venosus blood velocity in the second half of pregnancy. Ultrasound Obstet Gynecol 2013; 42(2): 245-6.
[46]
Demirturk F, Caliskan AC, Aytan H, Sahin S. A preliminary retrospective study about the relationship between ductus venosus Doppler indices, nuchal translucency (NT) and biochemical markers in the first and second trimester screening tests. Gynecol Endocrinol 2012; 28(5): 378-81.
[47]
Tongprasert F, Srisupundit K, Luewan S, Wanapirak C, Tongsong T. Normal reference ranges of ductus venosus Doppler indices in the period from 14 to 40 weeks’ gestation. Gynecol Obstet Invest 2012; 73(1): 32-7.
[48]
Stressig R, Kozlowski P, Froehlich S, et al. Assessment of the ductus venosus, tricuspid blood flow and the nasal bone in second-trimester screening for trisomy 21. Ultrasound Obstet Gynecol 2011; 37(4): 444-9.
[49]
Hung JH, Fu CY, Lu JH, Hung CY. Ductus venosus blood flow resistance and congenital heart defects in the second trimester. J Clin Ultrasound 2008; 36(2): 72-8.
[50]
Hecher K, Campbell S, Snijders R, Nicolaides K. Reference ranges for fetal venous and atrioventricular blood flow parameters. Ultrasound Obstet Gynecol 1994; 4(5): 381-90.
[51]
Fetal Medicine Foundation. Available at. https://fetalmedicine.org/fmf-certification/certificates-of-competence/ductus-venosus-flow Accessed October 30, 2017.
[52]
Teixeira LS, Leite J, Viegas MJ, et al. Ductus venosus Doppler velocimetry in the first trimester: A new finding. Ultrasound Obstet Gynecol 2008; 31(3): 261-5.
[53]
Kessler J, Rasmussen S, Hanson M, Kiserud T. Longitudinal reference ranges for ductus venosus flow velocities and waveform indices. Ultrasound Obstet Gynecol 2006; 28(7): 890-8.
[54]
Prefumo F, Risso D, Venturini PL, De Biasio P. Reference values for ductos venosus Doppler flow measurements at 10-14 weeks of gestation. Ultrasound Obstet Gynecol 2002; 20(1): 42-6.
[55]
Bahlmann F, Wellek S, Reinhardt I, Merz E, Steiner E, Welter C. Reference values of ductus venosus flow velocities and calculated waveform indices. Prenat Diagn 2000; 20(8): 623-34.
[56]
Baschat AA, Turan OM, Turan S. Ductus venosus blood-flow patterns: More than meets the eye? Ultrasound Obstet Gynecol 2012; 39(5): 598-9.
[57]
Abuhamad A, Chaoui R. Foetal cardiac function. In: Abuhamad A,
Chaoui R. A pratical guide to foetal echocardiography. 3rd Ed. Wolters
Kluwer. 2016; pp.178-86.
[58]
Sanapo L, Turan OM, Turan S, Ton J, Atlas M, Baschat AA. Correlation analysis of ductus venosus velocity indices and fetal cardiac function. Ultrasound Obstet Gynecol 2014; 43(5): 515-9.
[59]
Kiserud T, Hellevik LR, Eik-Nes SH, Angelsen BA, Blaas HG. Estimation of the pressure gradient across the fetal ductus venosus based on Doppler velocimetry. Ultrasound Med Biol 1994; 20: 225-32.
[60]
Papatheodorou SI, Evangelou E, Makrydimas G, Ioannidis JP. First-trimester ductus venosus screening for cardiac defects: A meta-analysis. BJOG 2011; 118(12): 1438-45.
[61]
Karadzov-Orlic N, Egic A, Filimonovic D, et al. Screening performances of abnormal first-trimester ductus venosus blood flow and increased nuchal translucency thickness in detection of major heart defects. Prenat Diagn 2015; 35(13): 1308-15.
[62]
Prats P, Ferrer Q, Comas C, Rodríguez I. Is the addition of the ductus venosus useful when screening for aneuploidy and congenital heart disease in fetuses with normal nuchal translucency? Fetal Diagn Ther 2012; 32(1 2): 138-43.
[63]
Wagner P, Sonek J, Eberle K, et al. First trimester screening for major cardiac defects based on the ductus venosus flow in fetuses with trisomy 21. Prenat Diagn 2018. Apr 16. [Epub ahead of print].
[64]
Alfirevic Z, Stampalija T, Dowswell T. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev 2017; 6: CD007529.
[65]
Cheema R, Bayoumi MZ, Gudmundsson S. Multivascular doppler surveillance in high risk pregnancies. J Matern Fetal Neonatal Med 2012; 25(7): 970-4.
[66]
Baschat AA. Ductus venosus doppler for fetal surveillance in high risk pregnancies. Clin Obstet Gynecol 2010; 53(4): 858-68.
[67]
Nicolaides KH. Nuchal translucency and other first-trimester sonographic markers of chromosomal abnormalities. Am J Obstet Gynecol 2004; 191(1): 45-67.
[68]
Matias A, Gomes C, Flack N, Montenegro N, Nicolaides KH. Screening for chromosomal abnormalities at 10-14 weeks: The role of ductus venosus blood flow. Ultrasound Obstet Gynecol 1998; 12(6): 380-4.
[69]
Maiz N, Valencia C, Emmanuel EE, Staboulidou I, Nicolaides KH. Screening for adverse pregnancy outcome by ductus venosus Doppler at 11-13+6 weeks of gestation. Obstet Gynecol 2008; 112(3): 598-605.
[70]
Maiz N, Nicolaides KH. Ductus venosus in the first trimester: contribution to screening of chromosomal, cardiac defects and monochorionic twin complications. Fetal Diagn Ther 2010; 28(2): 65-71.
[71]
Antolín E, Comas C, Torrents M, et al. The role of ductus venosus blood flow assessment in screening for chromosomal abnormalities at 10-16 weeks of gestation. Ultrasound Obstet Gynecol 2001; 17(4): 295-300.
[72]
Bilardo CM, Müller MA, Zikulnig L, Schipper M, Hecher K. Ductus venosus studies in fetuses at high risk for chromosomal or heart bnormalities: Relationship with nuchal translucency measurement and fetal outcome. Ultrasound Obstet Gynecol 2001; 17(4): 288-94.
[73]
Mäkikallio K, Acharya G, Erkinaro T, et al. Ductus venosus velocimetry in acute fetal acidemia and impending fetal death in a sheep model of increased placental vascular resistance. Am J Physiol Heart Circ Physiol 2010; 298(4): H1229-34.
[74]
Turan OM, Turan S, Berg C, et al. Duration of persistent abnormal ductus venosus flow and its impact on perinatal outcome in fetal growth restriction. Ultrasound Obstet Gynecol 2011; 38(3): 295-302.
[75]
Unterscheider J, Daly S, Geary MP, et al. Predictable progressive Doppler deterioration in IUGR: Does it really exist? Am J Obstet Gynecol 2013; 209(6): 539.e1-7.
[76]
Lees CC, Marlow N, van Wassenaer-Leemhuis A, et al. TRUFFLE study group. 2 year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): A randomised trial. Lancet 2015; 385(9983): 2162-72.
[77]
Frusca T, Todros T, Lees C, Bilardo CM. TRUFFLE Investigators. Outcome in early-onset fetal growth restriction is best combining computerized foetal heart rate analysis with ductus venosus doppler: Insights from the trial of umbilical and fetal flow in Europe. Am J Obstet Gynecol 2018; 218(2S): S783-9.
[78]
Djaafri F, Stirnemann J, Mediouni I, Colmant C, Ville Y. Twin-twin transfusion syndrome - What we have learned from clinical trials. Semin Fetal Neonatal Med 2017; 22(6): 367-75.
[79]
Perry H, Duffy JMN, Umadia O, Khalil A. International Collaboration to Harmonise Outcomes for Twin-Twin Transfusion Syndrome (CHOOSE). Outcome reporting across randomised trials and observational studies evaluating treatments for Twin-Twin Transfusion Syndrome: A systematic review. Ultrasound Obstet Gynecol 2018; 52(5): 577-85.
[80]
Stagnati V, Zanardini C, Fichera A, et al. Early prediction of twin-to-twin transfusion syndrome: Systematic review and meta-analysis. Ultrasound Obstet Gynecol 2017; 49(5): 573-82.
[81]
Wohlmuth C, Boudreaux D, Moise KJ Jr, et al. Cardiac pathophysiology in twin-twin transfusion syndrome: new insights into its evolution. Ultrasound Obstet Gynecol 2018; 51(3): 341-8.
[82]
Tachibana D, Glosemeyer P, Diehl W, et al. Time-interval analysis of ductus venosus flow velocity waveforms in twin-to-twin transfusion syndrome treated with laser surgery. Ultrasound Obstet Gynecol 2015; 45(5): 544-50.
[83]
Maruotti GM, Saccone G, Ciardulli A, Mazzarelli LL, Berghella V, Martinelli P. Absent ductus venosus: Case series from two tertiary centres. J Matern Fetal Neonatal Med 2017; 12: 1-6.
[84]
Thomas JT, Petersen S, Cincotta R, Lee-Tannock A, Gardener G. Absent ductus venosus--outcomes and implications from a tertiary centre. Prenat Diagn 2012; 32(7): 686-91.
[85]
Iliescu DG, Cara ML, Tudorache S, et al. Agenesis of ductus venosus in sequential first and second trimester screening. Prenat Diagn 2014; 34(11): 1099-105.
[86]
Berg C, Kamil D, Geipel A, et al. Absence of ductus venosus-importance of umbilical venous drainage site. Ultrasound Obstet Gynecol 2006; 28(3): 275-81.
[87]
Garcia-Delgado R, Garcia-Rodriguez R, Romero Requejo A, et al. Echographic features and perinatal outcomes in fetuses with congenital absence of ductus venosus. Acta Obstet Gynecol Scand 2017; 96(10): 1205-13.
[88]
Hofmann SR, Heilmann A, Häusler HJ, Kamin G, Nitzsche KI. Agenesis of the ductus venosus-A case with favorable outcome after early signs of cardiac failure. J Clin Ultrasound 2013; 41(3): 187-90.
[89]
Jacob S, Farr G, De Vun D, Takiff H, Mason A. Hepatic manifestations of familial patent ductus venosus in adults. Gut 1999; 45(3): 442-5.
[90]
Kamimatsuse A, Onitake Y, Kamei N, et al. Surgical intervention for patent ductus venosus. Pediatr Surg Int 2010; 26(10): 1025-30.
[91]
Llanos D, Armijo J, Bodas A, Vaquero E, de la Pedraja I, Arrazola J. Transjugular closure of a patent ductus venosus in a symptomatic 14-year-old boy using a vascular plug. J Pediatr 2014; 164(2): 426.e1-2.
[92]
Schierz IA, La Placa S, Giuffrè M, Montalbano G, Lenzo M, Corsello G. Transient hepatic nodular lesions associated with patent ductus venosus in preterm infants. Am J Perinatol 2011; 28(3): 177-80.
[93]
Chacko A, Kock C, Joshi JA, Mitchell L, Ahmad S. Patent ductus venosus presenting with cholestatic jaundice in an infant with successful trans-catheter closure using a vascular plug device. Indian J Radiol Imaging 2016; 26(3): 377-82.
[94]
Saito M, Seo Y, Yano Y, et al. Successful treatment using coil embolization of a symptomatic intrahepatic portosystemic venous shunt developing through a patent ductus venosus in a noncirrhotic adult. Intern Med 2013; 52(5): 555-9.
[95]
Hara Y, Sato Y, Yamamoto S, et al. Successful laparoscopic division of a patent ductus venosus: Report of a case. Surg Today 2013; 43(4): 434-8.
[96]
Macchi V, Porzionato A, Tiengo C, Parenti A, De Caro R. Persistence of embryonic pattern of hepatocaval venous junction and patent ductus venosus in Budd-Chiari syndrome. Clin Anat 2006; 19(7): 673-7.
[97]
Murayama K, Nagasaka H, Tate K, et al. Significant correlations between the flow volume of patent ductus venosus and early neonatal liver function: possible involvement of patent ductus venosus in postnatal liver function. Arch Dis Child Fetal Neonatal Ed 2006; 91(3): F175-9.
[98]
Alomari AI, Chaudry G, Fox VL, Fishman SJ, Buchmiller TL. Atypical manifestation of patent ductus venosus in a child: Intervening against a paradoxical presentation. J Vasc Interv Radiol 2009; 20(4): 537-42.
[99]
Sharma R, Crowley J, Squires R, et al. Neonatal acute liver failure complicated by patent ductus venosus: Diagnosis and management. Liver Transpl 2013; 19(9): 1049-52.
[100]
Yamaguchi H, Kosugiyama K, Honda S, Tadao O, Taketomi A, Iwata S. Down syndrome with patent ductus venosus and hepato-biliary-pancreatic abnormalities. Indian J Pediatr 2016; 83(1): 78-80.
[101]
Knisely AS. Patent ductus venosus and acute liver failure in the neonate: Consider neonatal hemochromatosis with liver scarring. Liver Transpl 2014; 20(1): 124.
[102]
Yoshimoto Y, Shimizu R, Saeki T, et al. Patent ductus venosus in children: A case report and review of the literature. J Pediatr Surg 2004; 39(1): E1-5.
[103]
Subramanian V, Kavassery MK, Sivasubramonian S, Sasidharan B. Percutaneous device closure of persistent ductus venosus presenting with hemoptysis. Ann Pediatr Cardiol 2013; 6(2): 173-5.
[104]
Kamata S, Kitayama Y, Usui N, et al. Patent ductus venosus with a hypoplastic intrahepatic portal system presenting intrapulmonary shunt: A case treated with banding of the ductus venosus. J Pediatr Surg 2000; 35(4): 655-7.
[105]
Aydinli M, Onal IK, Harmanci O, Ersoy O, Balkanci F, Bayraktar Y. A case of patent ductus venosus complicated with tumor-like lesions of the liver. J Natl Med Assoc 2008; 100(1): 108-11.
[106]
Toib A, Goldstein SB, Khanna G, et al. Spontaneous echocardiographic contrast associated with portosystemic shunt due to persistent patent ductus venosus. Congenit Heart Dis 2012; 7(3): E18-21.
Article Metrics
81
2