Pediatric and Developmental Pathology

, Volume 7, Issue 3, pp 237–249 | Cite as

Maternal Vascular Underperfusion: Nosology and Reproducibility of Placental Reaction Patterns

  • Raymond W. Redline
  • Theonia Boyd
  • Valarie Campbell
  • Scott Hyde
  • Cynthia Kaplan
  • T. Yee Khong
  • Heather R. Prashner
  • Brenda L. Waters
  • for the Society for Pediatric Pathology, Perinatal Section, Maternal Vascular Underperfusion Nosology Committee
Original Article

Abstract

Placental examination can be a useful tool for specifying the etiology, prognosis, and recurrence risk of pregnancy disorders. The purpose of this study was to test the reliability of a predetermined set of placental reaction patterns seen with maternal vascular underperfusion in the hope that this might provide a useful diagnostic framework for practicing pathologists. Study cases (14 with clinical and pathologic evidence of maternal underperfusion plus 6 controls) were evaluated for the presence or absence of 11 lesions by eight perinatal pathologists. After analysis of initial results, diagnostic criteria were refined and a second, overlapping set of cases was reviewed. The collective sensitivity, specificity, and efficiency of individual assessments for the 11 lesions relative to the group consensus ranged from 74–93% (22/33 > 90%). Reproducibility was measured by unweighted kappa-values and interpreted as follows: < 0.2 poor, 0.2–0.6 fair/moderate, > 0.6 substantial. Kappa values for lesions affecting villi and the intervillous space were increased syncytial knots (any −0.42, severe −0.50), villous agglutination (0.42), increased intervillous fibrin (0.25), and distal villous hypoplasia (0.57). Individual estimates of percent involvement for syncytial knots, intervillous fibrin, and distal villous hypoplasia were correlated with placental and fetal weight for gestational age. Extent of increased intervillous fibrin showed the strongest correlation with both placental weight (R = −0.64) and fetal weight (R = −0.45). Kappa values for lesions affecting maternal vessels and the implantation site were acute atherosis (0.50), mural hypertrophy of membrane arterioles (0.43), muscularized basal plate arteries (0.48), increased placental site giant cells (0.54), and immature intermediate trophoblast (0.36). Correlation of maternal vessel and implantation site lesions with the clinical diagnosis of preeclampsia showed that excessive placental site giant cells and immature intermediate trophoblast were more sensitive and efficient predictors, whereas atherosis and muscularized basal plate arteries were more specific. Kappa value for a thin umbilical cord, a possible indicator of fetal volume depletion, was 0.61. Reproducibility for a global impression of maternal vascular underperfusion, taking into account all of the above lesions, was moderate (kappa 0.54) and improved after inclusion of additional pathologic and clinical data (kappa 0.68). Adoption of this clearly defined, clinically relevant, and pathologically reproducible terminology could enhance clinicopathologic correlation and provide a more objective framework for future clinical research.

intrauterine growth retardation maternal vascular underperfusion placenta preeclampsia reproducibility uteroplacental insufficiency 

References

  1. 1.
    De Wolf, F, Brosens, I, Renaer, M 1980Fetal growth retardation and the maternal arterial supply of the human placenta in the absence of sustained hypertensionBr J Obstet Gynaecol87678684PubMedGoogle Scholar
  2. 2.
    Lackman, F, Capewell, V, Richardson, B, daSilva, O, Gagnon, R 2001The risks of spontaneous preterm delivery and perinatal mortality in relation to size at birth according to fetal versus neonatal growth standardsAm J Obstet Gynecol184946953CrossRefPubMedGoogle Scholar
  3. 3.
    Arias, F, Victorio, A, Cho, K, Kraus, FT 1997Placental histology and clinical characteristics of patients with preterm premature rupture of membranesObstet Gynecol89265271CrossRefPubMedGoogle Scholar
  4. 4.
    Naeye, RL 1989Pregnancy hypertension, placental evidences of low utero-placental blood flow and spontaneous premature deliveryHum Pathol20441444CrossRefPubMedGoogle Scholar
  5. 5.
    Lain, KY, Roberts, JM 2002Contemporary concepts of the pathogenesis and management of preeclampsiaJAMA28731833186CrossRefPubMedGoogle Scholar
  6. 6.
    Kaplan, C, Lowell, DM, Salafia, C 1991College of American Pathologists Conference XIX on The Examination of the Placenta: report of the working group on the definition of structural changes associated with abnormal function in the maternal/fetal/placental unit in the second and third trimestersArch Pathol Lab Med115709716PubMedGoogle Scholar
  7. 7.
    Langston, C, Kaplan, C, Macpherson, T,  et al. 1997Practice guideline for examination of the placentaArch Pathol Lab Med121449476PubMedGoogle Scholar
  8. 8.
    Gruenwald, P 1977The development of the placental lobular pattern in the human. Review and reinterpretation of the materialObstet Gynecol49728732PubMedGoogle Scholar
  9. 9.
    Landis, JR, Koch, GG 1977The measurement of observer agreement for categorical dataBiometrics33159174PubMedGoogle Scholar
  10. 10.
    Boyd, TK, Gang, DL, Lis, G, Juozokas, A, Pflueger, S 1999Normative values for placental weights (N = 15,463): Baystate Medical CenterMod Pathol121PGoogle Scholar
  11. 11.
    Dombrowski, MP, Wolfe, HM, Brans, YW, Saleh, AA, Sokol, RJ 1992Neonatal morphometry. Relation to obstetric, pediatric, and menstrual estimates of gestational ageAm J Dis Child146852856PubMedGoogle Scholar
  12. 12.
    Sun, CC, Revell, VO, Belli, AJ, Viscardi, RM 2002Discrepancy in pathologic diagnosis of placental lesionsArch Pathol Lab Med126706709PubMedGoogle Scholar
  13. 13.
    Khong, TY, Staples, A, Bendon, RW,  et al. 1995Observer reliability in assessing placental maturity by histologyJ Clin Pathol48420423PubMedGoogle Scholar
  14. 14.
    Khong, TY, Bendon, RW, Qureshi, F,  et al. 2000Chronic deciduitis in the placental basal plate: definition and inter-observer reliabilityHum Pathol31292295PubMedGoogle Scholar
  15. 15.
    Grether, JK, Eaton, A, Redline, R, Bendon, R, Benirschke, K, Nelson, K 1999Reliability of placental histology using archived specimensPaediat Perinat Epidemiol13489495CrossRefGoogle Scholar
  16. 16.
    Beebe, LA, Cowan, LD, Hyde, SR, Altshuler, G 2000Methods to improve the reliability of histopathological diagnoses in the placentaPaediatr Perinat Epidemiol14172178CrossRefPubMedGoogle Scholar
  17. 17.
    Redline R, Faye-Peterson O, Heller D, Qureshi F, Savell V, Vogler C. (2003) Amniotic fluid infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 6: 435–448CrossRefPubMedGoogle Scholar
  18. 18.
    Gruenwald, P 1975Fetal deprivation and placental pathology: concepts and relationshipsPerspect Pediatr Pathol2101149PubMedGoogle Scholar
  19. 19.
    Kingdom, J 1998Adriana and Luisa Castellucci Award Lecture 1997. Placental pathology in obstetrics: adaptation or failure of the villous treePlacenta19347351CrossRefPubMedGoogle Scholar
  20. 20.
    Jauniaux, E, Hempstock, J, Greenwold, N, Burton, GJ 2003Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnanciesAm J Pathol162115125PubMedGoogle Scholar
  21. 21.
    Tenney, B, Parker, F 1940The placenta in toxemia of pregnancyAm Obstet Gynecol3910001005Google Scholar
  22. 22.
    Tominaga, T, Page, EW 1966Accommodation of the human placenta to hypoxiaAm J Obstet Gynecol94679691PubMedGoogle Scholar
  23. 23.
    Mayhew, TM, Barker, BL 2001Villous trophoblast: morphometric perspectives on growth, differentiation, turnover and deposition of fibrin-type fibrinoid during gestationPlacenta22628638CrossRefPubMedGoogle Scholar
  24. 24.
    Redline, R 1999

    Disorders of the placental parenchyma

    Lewis, SHPerrin, E eds. Pathology of the PlacentaChurchill LivingstonePhiladelphia161184
    Google Scholar
  25. 25.
    Huppertz, B, Kingdom, J, Caniggia, I,  et al. 2003Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulationPlacenta24181190CrossRefPubMedGoogle Scholar
  26. 26.
    Altshuler, G, Russell, P, Ermocilla, R 1975The placental pathology of small-for-gestational age infantsAm J Obstet Gynecol121351359PubMedGoogle Scholar
  27. 27.
    Altshuler, G 1993A conceptual approach to placental pathology and pregnancy outcomeSemin Diagn Pathol10204221PubMedGoogle Scholar
  28. 28.
    Jackson, MR, Walsh, AJ, Morrow, RJ, Mullen, JB, Lye, SJ, Ritchie, JW 1995Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveformsAm J Obstet Gynecol172518525CrossRefPubMedGoogle Scholar
  29. 29.
    Karsdorp, VH, Dirks, BK, van der Linden, JC, van Vugt, JM, Baak, JP, van Geijn, HP 1996Placenta morphology and absent or reversed end diastolic flow velocities in the umbilical artery: a clinical and morphometrical studyPlacenta17393399CrossRefPubMedGoogle Scholar
  30. 30.
    Macara, L, Kingdom, JC, Kohnen, G, Bowman, AW, Greer, IA, Kaufmann, P 1995Elaboration of stem villous vessels in growth restricted pregnancies with abnormal umbilical artery Doppler waveformsBr J Obstet Gynaecol102807812PubMedGoogle Scholar
  31. 31.
    Krebs, C, Macara, LM, Leiser, R, Bowman, AW, Greer, IA, Kingdom, JC 1996Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous treeAm J Obstet Gynecol17515341542PubMedGoogle Scholar
  32. 32.
    Madazli, R, Somunkiran, A, Calay, Z, Ilvan, S, Aksu, MF 2003Histomorphology of the placenta and the placental bed of growth restricted foetuses and correlation with the Doppler velocimetries of the uterine and umbilical arteriesPlacenta24510516CrossRefPubMedGoogle Scholar
  33. 33.
    Khong, TY 1991The Roberston-Brosens-Dixon hypothesis: evidence for the role of haemochorial placentation in pregnancy successBr J Obstet Gynaecol9811951199PubMedGoogle Scholar
  34. 34.
    Kliman, HJ 2000Uteroplacental blood flow—the story of decidualization, menstruation, and trophoblast invasionAm J Pathol15717591768PubMedGoogle Scholar
  35. 35.
    Khong, TY, De Wolf, F, Robertson, WB, Brosens, I 1986Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infantsBr J Obstet Gynaecol9310491059PubMedGoogle Scholar
  36. 36.
    Barth Jr, WH, Genest, DR, Riley, LE, Frigoletto Jr, FD, Benacerraf, BR, Greene, MF 1996Uterine arcuate artery Doppler and decidual microvascular pathology in pregnancies complicated by type I diabetes mellitusUltrasound Obstet Gynecol898103CrossRefPubMedGoogle Scholar
  37. 37.
    Burstein, R, Berns, AW, Frankel, S, Blumenthal, HT 1965The occurrence of an immunopathologic vascular lesion in normal and abnormal pregnanciesAm J Obstet Gynecol927886PubMedGoogle Scholar
  38. 38.
    Kitzmiller JL, Watt N, Driscoll SG (1981) Decidual arteriopathy in hypertension and diabetes in pregnancy: immunofluorescent studies. Am J Obstet Gynecol 141:773–779PubMedGoogle Scholar
  39. 39.
    Redline, RW, Patterson, P 1995Preeclampsia is associated with an excess of proliferative immature intermediate trophoblastHum Pathol26594600PubMedGoogle Scholar
  40. 40.
    Lim, KH, Zhou, Y, Janatpour, M,  et al. 1997Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsiaAm J Pathol15118091818PubMedGoogle Scholar
  41. 41.
    Khong, TY 1991Acute atherosis in pregnancies complicated by hypertension, growth retardation, and diabetes melitusArch Pathol Lab Med115722725PubMedGoogle Scholar
  42. 42.
    Won, R, Oi, R, Gilbert, W 2001Placental decidual artery atherosis in severe preeclampsiaAm J Obstet Gynecol185S173CrossRefGoogle Scholar
  43. 43.
    Ness, RB, Roberts, JM 1996Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implicationsAm J Obstet Gynecol17513651370PubMedGoogle Scholar
  44. 44.
    Maynard, SE, Min, JY, Merchan, J,  et al. 2003Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsiaJ Clin Invest111649658CrossRefPubMedGoogle Scholar
  45. 45.
    Salafia, CM, Xenophon, J, Vintzileos, AM, Lerer, T, Silberman, L 1990Fetal growth and placental pathology in maternal hypertensive disordersClin Exp Hyper PregnB92741Google Scholar
  46. 46.
    Bruch, JF, Sibony, O, Benali, K, Challier, JC, Blot, P, Nessmann, C 1997Computerized microscope morphometry of umbilical vessels from pregnancies with intrauterine growth retardation and abnormal umbilical artery DopplerHum Pathol2811391145PubMedGoogle Scholar
  47. 47.
    Raio, L, Ghezzi, F, Di Naro, E,  et al. 1999Sonographic measurement of the umbilical cord and fetal anthropometric parametersEur J Obstet Gynecol Reprod Biol83131135CrossRefPubMedGoogle Scholar

Copyright information

© Society for Pediatric Pathology 2004

Authors and Affiliations

  • Raymond W. Redline
    • 1
  • Theonia Boyd
    • 2
  • Valarie Campbell
    • 3
  • Scott Hyde
    • 4
  • Cynthia Kaplan
    • 5
  • T. Yee Khong
    • 6
  • Heather R. Prashner
    • 7
  • Brenda L. Waters
    • 8
  • for the Society for Pediatric Pathology, Perinatal Section, Maternal Vascular Underperfusion Nosology Committee
  1. 1.Department of PathologyUniversity Hospitals of Cleveland and Case Western Reserve UniversityUSA
  2. 2.Department of PathologyBaystate Medical CenterSpringfieldUSA
  3. 3.Iowa Pathology AssociatesDes MoinesUSA
  4. 4.Department of PathologySt. Francis HospitalTulsaUSA
  5. 5.University HospitalStony BrookUSA
  6. 6.Department of HistopathologyWomen’s and Children’s HospitalNorth AdelaideAustralia
  7. 7.Department of PathologyUniversity of Texas Medical SchoolHoustonUSA
  8. 8.Department of PathologyFletcher Allen Health CareBurlingtonUSA

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