Association of Placental Histology with the Pulsatility Index of Fetal and Uteroplacental Vessels during Pregnancy and with Birthweight Z-Score
Main Article Content
Abstract
Aims: To compare macro- and microscopic features of the placenta with the pulsatility index (PI) of the uterine (UtA), umbilical (UA) and middle cerebral arteries at 20-24- and 34-38-weeks’ gestation, and with birthweight z-scores (BWZS).
Methods: Recruitment for the Safe Passage Study, which investigated the association of alcohol and tobacco use with stillbirth and sudden infant death syndrome, occurred from August 2007 to January 2015 at community clinics in Cape Town, South Africa. The population represents a predominantly homogenous population of pregnant women from a low socioeconomic residential area. This study is a further analysis of the data of the Safe Passage Study. It consists of 1205 singleton pregnancies for which placental histology was available, of whom 1035 had a known BWZS and 1022 and 979 had fetoplacental Doppler examinations performed at Tygerberg Academic Hospital at 20-24 and 34-38 weeks respectively. Features of the placenta were assessed according to international norms.
Results: Significantly higher ORs for the presence of individual and combined features of maternal vascular malperfusion (MVM) were found with lower BWZS and higher UtA PI values, more consistently than with higher UA PI values. Strongest associations were for a small placenta for gestational age (UtA OR 4.86 at 20-24 and 5.92 at 34-38 weeks; UA OR 5.33 at 20-24 and 27.01 at 34-38 weeks; low BWZS OR 0.31), for accelerated maturation (UtA OR 11.68 at 20-24 weeks and 18.46 at 34-38 weeks; low BWZS 0.61), for macroscopic infarction (UtA OR 6.08 at 20-24 weeks; UA OR 17.02 at 34-38 weeks; low BWZS OR 0.62) and for microscopic infarction (UtA OR 6.84 at 20-24 and 10.9 at 34-38 weeks; low BWZS OR 0.62).
Conclusion: There is considerable variability in the associations between individual features of MVM and increased UtA or UA PI and low BWZS. Although all MVM features currently carry equal weight in defining the condition of MVM, our data suggest that some should carry more weight than others. Macroscopic examination of the placenta may be helpful in identifying placental insufficiency as a small placenta for gestational age and macroscopic infarction were the features most strongly associated with outcomes.
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References
2. Ptacek I, Sebire NJ, Man JA, Brownbill P, Heazell AEP. Systematic review of placental pathology reported in association with stillbirth. Placenta. 2014;35(8):552–562.
3. Goldenberg RL, Saleem S, Pasha O, Harrison MS, McClure EM. Reducing stillbirths in low-income countries. Acta Obstet Gynecol Scand. 2016;95(2):135–143.
4. Redline RW. The clinical implications of placental diagnoses. Semin Perinatol. 2015;39(1):2–8.
5. Kingdom J, Huppertz B, Seaward G, Kaufmann P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol. 2000;92(1):35–43.
6. Kidron D, Bernheim J, Aviram R. Placental findings contributing to fetal death, a study of 120 stillbirths between 23 and 40 weeks gestation. Placenta. 2009;30(8):700–704.
7. Tiwari P, Gupta MM, Jain SL. Placental findings in singleton stillbirths: a case-control study from a tertiary-care center in India. J Perinat Med. 2021;50(6):753-762.
8. Ernst LM. Maternal vascular malperfusion of the placental bed. APMIS. 2018;126(7):551–560.
9. Paules C, Youssef L, Rovira C, et al. Distinctive patterns of placental lesions in pre-eclampsia vs small-for-gestational age and their association with fetoplacental Doppler. Ultrasound Obstet Gynecol. 2019;54(5):609–616.
10. Lloyd-Davies C, Collins SL, Burton GJ. Understanding the uterine artery Doppler waveform and its relationship to spiral artery remodelling. Placenta. 2021;105:78–84.
11. Ashwal E, Ferreira F, Mei-Dan E, et al. The accuracy of Fetoplacental Doppler in distinguishing between growth restricted and constitutionally small fetuses. Placenta. 2022;120:40–48.
12. Leppänen M, Ekholm E, Palo P, et al. Abnormal antenatal Doppler velocimetry and cognitive outcome in very-low-birth-weight infants at 2 years of age. Ultrasound Obstet Gynecol. 2010;36(2):178–185.
13. Perry H, Lehmann H, Mantovani E, Thilaganathan B, Khalil A. Correlation between central and uterine hemodynamics in hypertensive disorders of pregnancy. Ultrasound Obstet Gynecol. 2019;54(1):58–63.
14. Dukes KA, Burd L, Elliott AJ, et al. The Safe Passage Study: Design, methods, recruitment, and follow-up approach. Paediatr Perinat Epidemiol. 2014;28(5):455–465.
15. Boyd T, Wright C, Odendaal H, Elliott A, Sens M, Dunn F. The Stillbirth Classification System for the Safe Passage Study: Incorporating Mechanism, Etiology, and Recurrence. Pediatr Dev Pathol. 2017; 20 (2):120-132.
16. Odendaal H, Dukes KA, Elliott AJ, et al. Association of Prenatal Exposure to Maternal Drinking and Smoking with the Risk of Stillbirth. JAMA Netw Open. 2021;4(8):1–15.
17. Odendaal HJ, Brink LT, Nel DG, et al. Smoking and drinking habits of women in subsequent pregnancies after specific advice about the dangers of these exposures during pregnancy. S Afr Med J. 2020;110(11):1100–1104.
18. Geerts L, Theron AM, Grove D, Theron GB, Odendaal HJ. A community-based obstetric ultrasound service. Int J Gynecol Obstet. 2004;84(1):23–31.
19. Bhide A, Acharya G, Bilardo CM, et al. ISUOG (International Society of Ultrasound in Obstetrics and Gynecology) practice guidelines: Use of Doppler ultrasonography in obstetrics. Ultrasound Obstet Gynecol. 2013;41(2):233–239.
20. Odendaal H, Wright C, Schubert P, et al. Associations of maternal smoking and drinking with fetal growth and placental abruption. Eur J Obstet Gynecol Reprod Biol. 2020;253:95-102.
21. Odendaal H, Pattinson RC, Schubert P, et al. The key role of examining the placenta in establishing a probable cause for stillbirth. Placenta.2022:129:77-83.
22. Khong TY, Mooney EE, Ariel I, et al. Sampling and definitions of placental lesions Amsterdam placental workshop group consensus statement. Arch Pathol Lab Med. 2016;140(7):698–713.
23. Pinar H, Sung CJ, Oyer CE, Singer DB. Reference values for singleton and twin placental weights. Pediatr Pathol Lab Med. 1996;16(6):901–907.
24. Iskender C, Zergeroglu S, Kaymak O, Çelen S, Danisman N. Villitis of unknown aetiology: Clinical implications in preterm population. J Obstet Gynaecol. 2016;36(2):192–195.
25. Boog G. Chronic villitis of unknown etiology. Eur J Obstet Gynecol Reprod Biol. 2008;136(1):9–15.
26. Villar J, Papageorghiou AT, Pang R, et al. The likeness of fetal growth and newborn size across non-isolated populations in the INTERGROWTH-21st project: The fetal growth longitudinal study and newborn cross-sectional study. Lancet Diabetes Endocrinol. 2014;2(10):781–792.
27. Sbrana E, Suter MA, Abramovici AR, et al. Maternal tobacco use is associated with increased markers of oxidative stress in the placenta. Am J Obstet Gynecol. 2011;205(3):246.e1-246.e7.
28. Ratiu D, Hide-Moser K, Morgenstern B, et al. Doppler indices and notching assessment of uterine artery between the 19th and 22nd week of pregnancy in the prediction of pregnancy outcome. In Vivo. 2019;33(6):2199–2204.
29. Oviedo-Cruz H, Carrasco-Blancas ER, Cortés-Martínez MA. Reference values for uterine artery mean pulsatility index throughout pregnancy customized by parity, transvaginal measurement and blood pressure. Gac Med Mex. 2022;158(1):48–54.
30. Spinillo A, Gardella B, Adamo L, Muscettola G, Fiandrino G, Cesari S. Pathologic placental lesions in early and late fetal growth restriction. Acta Obstet Gynecol Scand. 2019;98(12):1585–1594.
31. Meher S, Hernandez-Andrade E, Basheer SN, Lees C. Impact of cerebral redistribution on neurodevelopmental outcome in small-for-gestational-age or growth-restricted babies: A systematic review. Ultrasound Obstet Gynecol. 2015;46(4):398–404.
32. Luzi G, Coata G, Caserta G, Cosmi E V., Di Renzo GC. Doppler velocimetry of different sections of the fetal middle cerebral artery in relation to perinatal outcome. J Perinat Med. 1996;24(4):327–334.
33. Velauthar L, Plana MN, Kalidindi M, et al. First-trimester uterine artery Doppler and adverse pregnancy outcome: A meta-analysis involving 55 974 women. Ultrasound Obstet Gynecol. 2014;43(5):500–507.
34. Odendaal HJ. Smoking and drinking during pregnancy. Obstet Gynaecol Forum. 2008;18(1):1–3.
35. Hernandez‐Andrade E, Huntley ES, Bartal MF, Soto‐Torres EE, Tirosh D, Jaiman S, Johnson A. Doppler evaluation of normal and abnormal placenta. Ultrasound Obst Gyn. 2022;60(1):28-41.
36. Khong TY, Mooney EE, Nikkels PG, Morgan TK, Gordijn SJ, editors. Pathology of the placenta: a practical guide. Springer International Publishing; 2019. https://doi.org/10.1007/978-3-319-97214-5
37. Parks WT. Manifestations of hypoxia in the second and third trimester placenta. Birth Defects Res. 2017;109(17):1345-1357.
38. Jaiman S, Romero R, Pacora P, Erez O, Jung E, Tarca AL, Bhatti G, Yeo L, Kim YM, Kim CJ, Kim JS. Disorders of placental villous maturation are present in one-third of cases with spontaneous preterm labor. J Perinat Med. 2021; 49(4):412-430.
39. Rotshenker-Olshinka K, Michaeli J, et al. Recurrent intrauterine growth restriction: characteristic placental histopathological features and association with prenatal vascular Doppler. Arch Gynecol Obstet. 2019;300(6):1583–1589.
40. Pinette MG, Loftus-Brault K, Nardi DA, Rodis JF. Maternal smoking and accelerated placental maturation. Obstet Gynecol. 1989;73(3 Pt 1):379-382.
41. Redline RW, Vik T, Heerema-McKenney A, Jamtoy AH, Ravishankar S, Ton Nu TN, Vogt C, Ng P, Nelson KB, Lydersen S, Oskoui M. Interobserver reliability for identifying specific patterns of placental injury as defined by the Amsterdam classification. Arch Pathol Lab Med. 2022;146(3):372-378.
42. Pacora P, Romero R, Jaiman S, et al. Mechanisms of death in structurally normal stillbirths. J Perinat Med. 2019;47(2):222–240.
43. Audette MC, Kingdom JC. Screening for fetal growth restriction and placental insufficiency. Semin Fetal Neonatal Med. 2018;23(2):119-125.
44. Ananth C V., Smulian JC, Demissie K, Vintzileos AM, Knuppel RA. Placental abruption among singleton and twin births in the United States: Risk factor profiles. Am J Epidemiol. 2001;153(8):771–778.
45. Ananth C V., Vintzileos AM. Ischemic placental disease: Epidemiology and risk factors. Eur J Obstet Gynecol Reprod Biol. 2011;159(1):77–82.
46. Ananth C V. Ischemic placental disease: A unifying concept for preeclampsia, intrauterine growth restriction, and placental abruption. Semin Perinatol. 2014;38(3):131–132.
47. Marsden L, Comstock J. Fetal thrombotic vasculopathy. Journal of Fetal Medicine. 2015 Sep;2:121-125.
48. Ganer Herman H, Barber E, Gasnier R, Gindes L, Bar J, Schreiber L, et al. Placental pathology and neonatal outcome in small for gestational age pregnancies with and without abnormal umbilical artery Doppler flow. Eur J Obstet Gynecol Reprod Biol. 2018 Mar;222:52-56.