Top

Published in:

01-12-2019 | Intrauterine Growth Restriction | Maternal-Fetal Medicine

Recurrent intrauterine growth restriction: characteristic placental histopathological features and association with prenatal vascular Doppler

Authors: Keren Rotshenker-Olshinka, Jennia Michaeli, Naama Srebnik, Sveta Terlezky, Letizia Schreiber, Rivka Farkash, Sorina Grisaru Granovsky

Published in: Archives of Gynecology and Obstetrics | Issue 6/2019

Abstract

Purpose

Intrauterine growth restriction (IUGR) is a leading cause of perinatal morbidity and mortality, carrying a 20% recurrence rate. The placental disease is a cardinal factor among IUGR underlying processes. This study describes placental histopathological features (HPf) characteristic of recurrent IUGR (rIUGR) and assesses association with antenatal Doppler studies.

Methods

We conducted a retrospective case–control study, between the years 2005–2016, evaluating 34 placentae of 17 women with rIUGR, and 59 placentae of a gestational age-matched control. Doppler studies within a week prior to delivery were analyzed for the rIUGR group.

Results

Placental HPf characteristic of rIUGR is maternal and fetal vascular malperfusion lesions; maternal accelerated villous maturation and villous infarcts, repetitive feature rate 88.8% (95% CI 37.2–97), and fetal chorionic plate/stem villous thrombi, repetitive feature rate 66.6% (95% CI 30–90.3). Among women with abnormal Doppler, 83.3% had a placenta HPf of maternal vascular malperfusion lesions and 66.7% presented with a hypertensive disorder.

Conclusions

Women with rIUGR are a unique group of patients characterized by repetitive placental HPf of both maternal and fetal vascular malperfusion lesions. Specifically, maternal vascular malperfusion lesions are associated with abnormal Doppler findings. In conclusion, characteristic placental HPf may serve as predictors of future IUGR recurrence, thus offering early recognition of pregnancies that require “high-risk” antenatal care.

Wolfe HM, Gross TL, Sokol RJ (1987) Recurrent small for gestational age birth: perinatal risks and outcomes. Am J Obstet Gynecol 157:288–293CrossRef

Regev RH, Lusky A, Dolfin T, Litmanovitz I, Arnon S, Reichman B (2003) Israel Neonatal Network, Excess mortality and morbidity among small-for-gestational-age premature infants: a population-based study. J Pediatr 143:186–191. https://doi.org/10.1067/S0022-3476(03)00181-1 CrossRefPubMed

Barker DJP (2006) Adult consequences of fetal growth restriction. Clin Obstet Gynecol 49:270–283CrossRef

Platz E, Newman R (2008) Diagnosis of IUGR: traditional biometry. Semin Perinatol 32:140–147. https://doi.org/10.1053/j.semperi.2008.02.002 CrossRefPubMed

Berghella V (2007) Prevention of recurrent fetal growth restriction. Obstet Gynecol 110:904–912. https://doi.org/10.1097/01.AOG.0000267203.55718.aa CrossRefPubMed

American College of Obstetricians and Gynecologists (2013) Practice bulletin No. 134. Obstet Gynecol 121:1122–1133. https://doi.org/10.1097/01.aog.0000429658.85846.f9 CrossRef

Voskamp BJ, Kazemier BM, Ravelli ACJ, Schaaf J, Mol BWJ, Pajkrt E (2013) Recurrence of small-for-gestational-age pregnancy: analysis of first and subsequent singleton pregnancies in The Netherlands. Am J Obstet Gynecol 208:374.e1–374.e6. https://doi.org/10.1016/j.ajog.2013.01.045 CrossRef

Royal College of Obstetricians and Gynaecologists (2013) The Investigation and management of the small-for-gestational-age fetus. RCOG, London, UK (Green-Top Guideline no. 31)

Gabbe SG (n.d) Obstetrics: normal and problem pregnancies

10.

Roberts DJ, Post MD (2008) The placenta in pre-eclampsia and intrauterine growth restriction. J Clin Pathol 61:1254–1260. https://doi.org/10.1136/jcp.2008.055236 CrossRefPubMed

11.

Redline RW (2015) Classification of placental lesions. Am J Obstet Gynecol 213:S21–S28. https://doi.org/10.1016/j.ajog.2015.05.056 CrossRefPubMed

12.

Aviram R, Bs T, Kidron D (2010) Placental aetiologies of foetal growth restriction: clinical and pathological differences. Early Hum Dev 86:59–63. https://doi.org/10.1016/j.earlhumdev.2010.01.020 CrossRefPubMed

13.

Gunyeli I, Erdemoglu E, Ceylaner S, Zergeroglu S, Mungan T (2011) Histopathological analysis of the placental lesions in pregnancies complicated with IUGR and stillbirths in comparison with noncomplicated pregnancies. J Turkish Ger Gynecol Assoc 12:75–79. https://doi.org/10.5152/jtgga.2011.19 CrossRef

14.

Parant O, Capdet J, Kessler S, Aziza J, Berrebi A (2009) Chronic intervillositis of unknown etiology (CIUE): relation between placental lesions and perinatal outcome. Eur J Obstet Gynecol Reprod Biol 143:9–13. https://doi.org/10.1016/j.ejogrb.2008.06.012 CrossRefPubMed

15.

Nowak C, Joubert M, Jossic F, Masseau A, Hamidou M, Philippe H-J, Le Vaillant C (2016) Perinatal prognosis of pregnancies complicated by placental chronic villitis or intervillositis of unknown etiology and combined lesions: about a series of 178 cases. Placenta 44:104–108. https://doi.org/10.1016/j.placenta.2016.04.017 CrossRefPubMed

16.

Dollberg S, Haklai Z, Mimouni FB, Gorfein I, Gordon E-S (2005) Birth weight standards in the live-born population in Israel. Isr Med Assoc J 7:311–314PubMed

17.

Kovo M, Schreiber L, Ben-Haroush A, Wand S, Golan A, Bar J (2010) Placental vascular lesion differences in pregnancy-induced hypertension and normotensive fetal growth restriction. Am J Obstet Gynecol 202:561.e1–561.e5. https://doi.org/10.1016/j.ajog.2010.01.012 CrossRef

18.

Stocker JT, Dehner LP, Husain AN (2011) Stocker &. Dehner’s pediatric pathology. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia

19.

Khong TY, Mooney EE, Ariel I, Balmus NCM, Boyd TK, Brundler M-A, Derricott H, Evans MJ, Faye-Petersen OM, Gillan JE, Heazell AEP, Heller DS, Jacques SM, Keating S, Kelehan P, Maes A, McKay EM, Morgan TK, Nikkels PGJ, Parks WT, Redline RW, Scheimberg I, Schoots MH, Sebire NJ, Timmer A, Turowski G, van der Voorn JP, van Lijnschoten I, Gordijn SJ (2016) Sampling and definitions of placental lesions: Amsterdam placental workshop group consensus statement. Arch Pathol Lab Med 140:698–713. https://doi.org/10.5858/arpa.2015-0225-CC CrossRefPubMed

20.

Gosling RG, Dunbar G, King DH, Newman DL, Side CD, Woodcock JP, Fitzgerald DE, Keates JS, Macmillan D (1971) The quantitative analysis of occlusive peripheral arterial disease by a non-intrusive ultrasonic technique. Angiology 22:52–55. https://doi.org/10.1177/000331977102200109 CrossRefPubMed

21.

Arduini D, Rizzo G (1990) Normal values of Pulsatility Index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med 18:165–172CrossRef

22.

Acharya G, Wilsgaard T, Berntsen GKR, Maltau JM, Kiserud T (2005) Reference ranges for serial measurements of umbilical artery Doppler indices in the second half of pregnancy. Am J Obstet Gynecol 192:937–944. https://doi.org/10.1016/j.ajog.2004.09.019 CrossRefPubMed

23.

Vedmedovska N, Rezeberga D, Teibe U, Melderis I, Donders GGG (2011) Placental pathology in fetal growth restriction. Eur J Obstet Gynecol Reprod Biol 155:36–40. https://doi.org/10.1016/j.ejogrb.2010.11.017 CrossRefPubMed

24.

Redline RW, Ariel I, Baergen RN, deSa DJ, Kraus FT, Roberts DJ, Sander CM (2004) Fetal vascular obstructive lesions: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 7:443–452. https://doi.org/10.1007/s10024-004-2020-x CrossRefPubMed

25.

Burton GJ, Jauniaux E (2018) Development of the human placenta and fetal heart: synergic or independent? Front Physiol 9:373. https://doi.org/10.3389/fphys.2018.00373 CrossRefPubMedPubMedCentral

26.

Scifres CM, Nelson DM (2009) Intrauterine growth restriction, human placental development and trophoblast cell death. J Physiol 587:3453–3458. https://doi.org/10.1113/jphysiol.2009.173252 CrossRefPubMedPubMedCentral

27.

Burton GJ, Charnock-Jones DS, Jauniaux E (2009) Regulation of vascular growth and function in the human placenta. Reproduction 138:895–902. https://doi.org/10.1530/REP-09-0092 CrossRefPubMed

28.

Turowski G, Berge LN, Helgadottir LB, Jacobsen E-M, Roald B (2012) A new, clinically oriented, unifying and simple placental classification system. Placenta 33:1026–1035. https://doi.org/10.1016/j.placenta.2012.10.002 CrossRefPubMed

29.

Park SY, Kim MY, Kim YJ, Chun YK, Kim HS, Kim HS, Hong SR (2002) Placental pathology in intrauterine growth retardation. Korean J Pathol 36:30–37

30.

Blair E, de Groot J, Nelson KB (2011) Placental infarction identified by macroscopic examination and risk of cerebral palsy in infants at 35 weeks of gestational age and over. Am J Obstet Gynecol 205:124.e1–124.e7CrossRef

31.

Redline RW (2008) Placental pathology: a systematic approach with clinical correlations. Placenta 29:86–91. https://doi.org/10.1016/j.placenta.2007.09.003 CrossRef

32.

Nordenvall M, Sandstedt B, Ulmsten U (1988) Relationship between placental shape, cord insertion, lobes and gestational outcome. Acta Obstet Gynecol Scand 67:611–616. https://doi.org/10.3109/00016348809004273 CrossRefPubMed

33.

Burton GJ, Jauniaux E (2018) Pathophysiology of placental-derived fetal growth restriction. Am J Obstet Gynecol 218:S745–S761. https://doi.org/10.1016/j.ajog.2017.11.577 CrossRefPubMed

34.

Barut F, Barut A, Gun BD, Kandemir NO, Harma MI, Harma M, Aktunc E, Ozdamar SO (2010) Intrauterine growth restriction and placental angiogenesis. Diagn Pathol 5:24. https://doi.org/10.1186/1746-1596-5-24 CrossRefPubMedPubMedCentral

35.

Chaiworapongsa T, Romero R, Whitten AE, Korzeniewski SJ, Chaemsaithong P, Hernandez-Andrade E, Yeo L, Hassan SS (2016) The use of angiogenic biomarkers in maternal blood to identify which SGA fetuses will require a preterm delivery and mothers who will develop pre-eclampsia. J Matern Neonatal Med 29:1214–1228. https://doi.org/10.3109/14767058.2015.1048431 CrossRef

36.

Tamblyn JA, Lissauer DM, Powell R, Cox P, Kilby MD (2013) The immunological basis of villitis of unknown etiology—review. Placenta 34:846–855. https://doi.org/10.1016/j.placenta.2013.07.002 CrossRefPubMed

37.

Baschat AA (2004) Doppler application in the delivery timing of the preterm growth-restricted fetus: another step in the right direction. Ultrasound Obstet Gynecol 23:111–118. https://doi.org/10.1002/uog.989 CrossRefPubMed

38.

Frusca T, Todros T, Lees C, Bilardo CM, Hecher K, Visser GHA, Papageorghiou AT, Marlow N, Thilaganathan B, van Wassenaer-Leemhuis A, Marsal K, Arabin B, Brezinka C, Derks JB, Diemert A, Duvekot JJ, Ferrazzi E, Ganzevoort JW, Martinelli P, Ostermayer E, Schlembach D, Valensise H, Thornton J, Wolf H (2018) Outcome in early-onset fetal growth restriction is best combining computerized fetal heart rate analysis with ductus venosus Doppler: insights from the Trial of Umbilical and Fetal Flow in Europe. Am J Obstet Gynecol 218:S783–S789. https://doi.org/10.1016/j.ajog.2017.12.226 CrossRefPubMed

39.

Romo A, Carceller R, Tobajas J (2009) Intrauterine growth retardation (IUGR): epidemiology and etiology. Pediatr Endocrinol Rev 6(Suppl 3):332–336PubMed

40.

Kovo M, Schreiber L, Elyashiv O, Ben-Haroush A, Abraham G, Bar J (2015) Pregnancy outcome and placental findings in pregnancies complicated by fetal growth restriction with and without preeclampsia. Reprod Sci 22:316–321. https://doi.org/10.1177/1933719114542024 CrossRefPubMed

41.

Hermansen MC (2001) Nucleated red blood cells in the fetus and newborn. Arch Dis Child Fetal Neonatal Ed 84:F211–F215. https://doi.org/10.1136/FN.84.3.F211 CrossRefPubMedPubMedCentral

42.

Wong SF, Chow KM, Ho LC (2002) The relative risk of “fetal distress” in pregnancy associated with meconium-stained liquor at different gestation. J Obstet Gynaecol (Lahore) 22:594–599. https://doi.org/10.1080/0144361021000020333 CrossRef

43.

Altshuler G, Hyde S (1989) Meconium-induced vasocontraction: a potential cause of cerebral and other fetal hypoperfusion and of poor pregnancy outcome. J Child Neurol 4:137–142. https://doi.org/10.1177/088307388900400214 CrossRefPubMed

44.

Huetz N, Triau S, Leboucher B, Sentilhes L, Hanf M, Nguyen S, Flamant C, Roze JC, Gascoin G, Association of severe placental inflammation with death prior to discharge and cerebral palsy in preterm infants. (n.d.). https://doi.org/10.1111/1471-0528.14210

45.

Sapir AZ, Khayyat I, Rabinowitz R, Samueloff A, Drukker L, Sela HY (2017) New Israeli sonographic estimated fetal weight growth curves as compared to current birth weight growth curves: on what should diagnosis of intrauterine growth disorders be based? Isr Med Assoc J 19:604–609PubMed

46.

Roberge S, Nicolaides K, Demers S, Hyett J, Chaillet N, Bujold E (2017) The role of aspirin dose on the prevention of preeclampsia and fetal growth restriction: systematic review and meta-analysis. Am J Obstet Gynecol 216:110–120.e6. https://doi.org/10.1016/j.ajog.2016.09.076 CrossRefPubMed

Title: Recurrent intrauterine growth restriction: characteristic placental histopathological features and association with prenatal vascular Doppler
Authors: Keren Rotshenker-Olshinka
Jennia Michaeli
Naama Srebnik
Sveta Terlezky
Letizia Schreiber
Rivka Farkash
Sorina Grisaru Granovsky
Publication date: 01-12-2019
Publisher: Springer Berlin Heidelberg
Keyword: Intrauterine Growth Restriction
Published in: Archives of Gynecology and Obstetrics / Issue 6/2019
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI: https://doi.org/10.1007/s00404-019-05339-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Recurrent intrauterine growth restriction: characteristic placental histopathological features and association with prenatal vascular Doppler

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 6/2019

Struma ovarii with atypical features and synchronous primary thyroid cancer: a case report and review of the literature

Hemorrhagic morbidity in placenta accreta spectrum with and without placenta previa

Response to “Letter to the Editor” by Federico Prefumo

Endometriosis reduces ovarian response in controlled ovarian hyperstimulation independent of AMH, AFC, and women’s age measured by follicular output rate (FORT) and number of oocytes retrieved

Long interpregnancy interval and mode of delivery

Effect of embryo selection based morphokinetics on IVF/ICSI outcomes: evidence from a systematic review and meta-analysis of randomized controlled trials