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The Journal of Maternal-Fetal & Neonatal Medicine Volume 28, 2015 - Issue 13
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Original Article

Placental lesions associated with acute atherosis

Yeon Mee KimDepartment of Pathology, Haeundae Paik Hospital, Inje University College of Medicine, Busan, Korea, Correspondence[email protected]
,
Piya ChaemsaithongPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA,
,
Roberto RomeroPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, MI, USA, ;Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA, Correspondence[email protected]
,
Majid ShamanPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA,
,
Chong Jai KimPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Pathology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea,
,
Jung-Sun KimPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Pathology, Samsung Medical Center, University of Sungkyunkwan School of Medicine, Seoul, Korea,
,
Faisal QureshiPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Pathology, Harper University Hospital, Detroit, MI, USA, and ;Department of Pathology, Wayne State University, Detroit, MI, USA
,
Suzanne M. JacquesPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Pathology, Harper University Hospital, Detroit, MI, USA, and ;Department of Pathology, Wayne State University, Detroit, MI, USA
,
Ahmed I. AhmedPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA,
,
Tinnakorn ChaiworapongsaPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA,
,
Sonia S. HassanPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA,
,
Lami YeoPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA,
&
Steven J. KorzeniewskiPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD and Detroit, MI, USA, ;Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA, ;Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA,
show all
Pages 1554-1562 | Received 30 Jul 2014, Accepted 29 Aug 2014, Published online: 30 Oct 2014

References

  • Hertig AT. Vascular pathology in the hypertensive albuminuric toxemias of pregnancy. Clinics 1945;4:602–14
  • Sexton LI, Hertig AT, Reid DE, et al. Premature separation of the normally implanted placenta; a clinicopathological study of 476 cases. Am J Obstet Gynecol 1950;59:13–24
  • Zeek PM, Assali NS. Vascular changes in the decidua associated with eclamptogenic toxemia of pregnancy. Am J Clin Pathol 1950;20:1099–109
  • Maqueo M, Chavezazuela J, Dosaldelavega M. Placental pathology in eclampsia and preeclampsia. Obstet Gynecol 1964;24:350–56
  • Driscoll SG. The pathology of pregnancy complicated by diabetes mellitus. Med Clin North Am 1965;49:1053–67
  • Robertson WB, Brosens I, Dixon HG. The pathological response of the vessels of the placental bed to hypertensive pregnancy. J Pathol Bacteriol 1967;93:581–92
  • Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972;1:177–91
  • Brosens I, Renaer M. On the pathogenesis of placental infarcts in pre-eclampsia. J Obstet Gynaecol Br Commonw 1972;79:794–99
  • Emmrich P, Birke R, Godel E. Morphology of myometrial and decidual arteries in normal pregnancy, in toxemia of pregnancy, and in maternal diabetes (author's transl). Pathol Microbiol (Basel) 1975;43:38–61
  • De Wolf F, Robertson WB, Brosens I. The ultrastructure of acute atherosis in hypertensive pregnancy. Am J Obstet Gynecol 1975;123:164–74
  • Robertson WB, Brosens I, Dixon G. Uteroplacental vascular pathology. Eur J Obstet Gynecol Reprod Biol 1975;5:47–65
  • Robertson WB, Brosens I, Dixon G. Maternal uterine vascular lesions in the hypertensive complications of pregnancy. Perspect Nephrol Hypertens 1976;5:115–27
  • De Wolf F, Brosens I, Renaer M. Fetal growth retardation and the maternal arterial supply of the human placenta in the absence of sustained hypertension. Br J Obstet Gynaecol 1980;87:678–85
  • Abramowsky CR, Vegas ME, Swinehart G, et al. Decidual vasculopathy of the placenta in lupus erythematosus. N Engl J Med 1980;303:668–72
  • Kitzmiller JL, Watt N, Driscoll SG. Decidual arteriopathy in hypertension and diabetes in pregnancy: immunofluorescent studies. Am J Obstet Gynecol 1981;141:773–79
  • Sheppard BL, Bonnar J. An ultrastructural study of utero-placental spiral arteries in hypertensive and normotensive pregnancy and fetal growth retardation. Br J Obstet Gynaecol 1981;88:695–705
  • De Wolf F, Carreras LO, Moerman P, et al. Decidual vasculopathy and extensive placental infarction in a patient with repeated thromboembolic accidents, recurrent fetal loss, and a lupus anticoagulant. Am J Obstet Gynecol 1982;142:829–34
  • Hustin J, Foidart JM, Lambotte R. Maternal vascular lesions in pre-eclampsia and intrauterine growth retardation: light microscopy and immunofluorescence. Placenta 1983;4:489–98
  • Althabe O, Labarrere C, Telenta M. Maternal vascular lesions in placentae of small-for-gestational-age infants. Placenta 1985;6:265–76
  • Labarrere C, Alonso J, Manni J, et al. Immunohistochemical findings in acute atherosis associated with intrauterine growth retardation. Am J Reprod Immunol Microbiol 1985;7:149–55
  • Labarrere C, Althabe O. Chronic villitis of unknown etiology and maternal arterial lesions in preeclamptic pregnancies. Eur J Obstet Gynecol Reprod Biol 1985;20:1–11
  • Khong TY, De Wolf F, Robertson WB, et al. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986;93:1049–59
  • McFadyen IR, Price AB, Geirsson RT. The relation of birthweight to histological appearances in vessels of the placental bed. Br J Obstet Gynaecol 1986;93:476–81
  • Labarrere CA, Catoggio LJ, Mullen EG, et al. Placental lesions in maternal autoimmune diseases. Am J Reprod Immunol Microbiol 1986;12:78–86
  • Khong TY, Pearce JM, Robertson WB. Acute atherosis in preeclampsia: maternal determinants and fetal outcome in the presence of the lesion. Am J Obstet Gynecol 1987;157:360–63
  • Labarrere CA. Acute atherosis. A histopathological hallmark of immune aggression? Placenta 1988;9:95–108
  • Frusca T, Morassi L, Pecorelli S, et al. Histological features of uteroplacental vessels in normal and hypertensive patients in relation to birthweight. Br J Obstet Gynaecol 1989;96:835–39
  • Khong TY. Acute atherosis in pregnancies complicated by hypertension, small-for-gestational-age infants, and diabetes mellitus. Arch Pathol Lab Med 1991;115:722–25
  • Meekins JW, Pijnenborg R, Hanssens M, et al. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994;101:669–74
  • Meekins JW, Pijnenborg R, Hanssens M, et al. Immunohistochemical detection of lipoprotein(a) in the wall of placental bed spiral arteries in normal and severe preeclamptic pregnancies. Placenta 1994;15:511–24
  • Salafia CM, Parke AL. Placental pathology in systemic lupus erythematosus and phospholipid antibody syndrome. Rheum Dis Clin North Am 1997;23:85–97
  • Brosens I, Dixon HG, Robertson WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977;84:656–63
  • Gerretsen G, Huisjes HJ, Elema JD. Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol 1981;88:876–81
  • Nayar R, Lage JM. Placental changes in a first trimester missed abortion in maternal systemic lupus erythematosus with antiphospholipid syndrome; a case report and review of the literature. Hum Pathol 1996;27:201–6
  • Hayati AR, Azizah A, Wahidah A. Incidence of acute atherosis in complete molar pregnancy. Malays J Pathol 1998;20:113–114
  • Khong TY, Hague WM. The placenta in maternal hyperhomocysteinaemia. Br J Obstet Gynaecol 1999;106:273–78
  • Ogishima D, Matsumoto T, Nakamura Y, et al. Placental pathology in systemic lupus erythematosus with antiphospholipid antibodies. Pathol Int 2000;50:224–29
  • Sebire NJ, Rees H, Paradinas F, et al. Extravillus endovascular implantation site trophoblast invasion is abnormal in complete versus partial molar pregnancies. Placenta 2001;22:725–28
  • Moldenhauer JS, Stanek J, Warshak C, et al. The frequency and severity of placental findings in women with preeclampsia are gestational age dependent. Am J Obstet Gynecol 2003;189:1173–77
  • Kraus FT, Redline RW, Gersell DJ, et al. Circulatory problems: thrombi and other vascular lesions. In: King DW, ed. Placental pathology, 1st ed. Washington DC: American Registry of Pathology; 2004:117–56
  • Faye-Petersen O, Heller DS, Joshi VV. Histologic lesions of the placenta: villi, fetal stem arteries, intervillous space and maternal arteries in decidua. In: Faye-Petersen O, Heller DS, Joshi VV, eds. Handbook of placental pathology, 2nd ed. United Kingdom: Taylor & Francis; 2006:53–78
  • Fox H, Sebire NJ. Histological abnormalities of the placenta. In: Fox H, Sebire NJ, eds. Pathology of the placenta, 3rd ed. China: Elsevier; 2007:147–86
  • Harsem NK, Roald B, Braekke K, et al. Acute atherosis in decidual tissue: not associated with systemic oxidative stress in preeclampsia. Placenta 2007;28:958–64
  • Brosens I, Khong TY. Defective spiral artery remodeling. In: Pijnenborg R, Brosens I, Romero R, eds. Placental bed disorders. Cambridge, UK: Cambridge University Press; 2010:11–21
  • Staff AC, Dechend R, Pijnenborg R. Learning from the placenta: acute atherosis and vascular remodeling in preeclampsia-novel aspects for atherosclerosis and future cardiovascular health. Hypertension 2010;56:1026–34
  • Stevens DU, Al-Nasiry S, Bulten J, et al. Decidual vasculopathy in preeclampsia: lesion characteristics relate to disease severity and perinatal outcome. Placenta 2013;34:805–9
  • Staff AC, Dechend R, Redman CW. Review: preeclampsia, acute atherosis of the spiral arteries and future cardiovascular disease: two new hypotheses. Placenta 2013;34:S73–78
  • Staff AC, Johnsen GM, Dechend R, et al. Preeclampsia and uteroplacental acute atherosis: immune and inflammatory factors. J Reprod Immunol 2014;101–102:120–26
  • Staff AC, Redman CW. IFPA Award in Placentology Lecture: preeclampsia, the decidual battleground and future maternal cardiovascular disease. Placenta 2014;35:S26–31
  • Kim YM, Chaemsaithong P, Romero R, et al. The frequency of acute atherosis in normal pregnancy and preterm labor, preeclampsia, small for gestational age, fetal death and mid-trimester spontaneous abortion. J Matern Fetal Neonatal Med (submitted). 2014. (in press)
  • Redline RW, Heller D, Keating S, et al. Placental diagnostic criteria and clinical correlation–a workshop report. Placenta 2005;26:S114–17
  • Ananth CV, Vintzileos AM. Maternal-fetal conditions necessitating a medical intervention resulting in preterm birth. Am J Obstet Gynecol 2006;195:1557–63
  • Ananth CV, Smulian JC, Vintzileos AM. Ischemic placental disease: maternal versus fetal clinical presentations by gestational age. J Matern Fetal Neonatal Med 2010;23:887–93
  • Ananth CV, Vintzileos AM. Ischemic placental disease: epidemiology and risk factors. Eur J Obstet Gynecol Reprod Biol 2011;159:77–82
  • Ananth CV. Ischemic placental disease: a unifying concept for preeclampsia, intrauterine growth restriction, and placental abruption. Semin Perinatol 2014;38:131–2
  • Kim CJ, Romero R, Kusanovic JP, et al. The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth. Modern Pathol 2010;23:1000–11
  • Redline RW. Villitis of unknown etiology: noninfectious chronic villitis in the placenta. Hum Pathol 2007;38:1439–46
  • Kim MJ, Romero R, Kim CJ, et al. Villitis of unknown etiology is associated with a distinct pattern of chemokine up-regulation in the feto-maternal and placental compartments: implications for conjoint maternal allograft rejection and maternal anti-fetal graft-versus-host disease. J Immunol 2009;182:3919–27
  • Khong TY, Bendon RW, Qureshi F, et al. Chronic deciduitis in the placental basal plate: definition and interobserver reliability. Hum Pathol 2000;31:292–95
  • Roberts DJ, Post MD. The placenta in pre-eclampsia and intrauterine growth restriction. J Clin Pathol 2008;61:1254–60
  • Pijnenborg R, Brosens I. Deep trophoblast invasion and spiral artery remodeling. In: Pijnenborg R, Brosens I, Romero R, eds. Placental bed disorders. Cambridge: Cambridge University Press; 2010:97–108
  • Ogge G, Chaiworapongsa T, Romero R, et al. Placental lesions associated with maternal underperfusion are more frequent in early-onset than in late-onset preeclampsia. J Perinat Med 2011;39:641–52
  • Pathak S, Lees CC, Hackett G, et al. Frequency and clinical significance of placental histological lesions in an unselected population at or near term. Virchows Arch 2011;459:565–72
  • Brosens I, Pijnenborg R, Vercruysse L, et al. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 2011;204:193–201
  • Khong Y, Brosens I. Defective deep placentation. Best Pract Res Clin Obstet Gynaecol 2011;25:301–11
  • Pijnenborg R, Vercruysse L, Brosens I. Deep placentation. Best Pract Res Clin Obstet Gynaecol 2011;25:273–85
  • Soto E, Romero R, Kusanovic JP, et al. Late-onset preeclampsia is associated with an imbalance of angiogenic and anti-angiogenic factors in patients with and without placental lesions consistent with maternal underperfusion. J Matern Fetal Neonatal Med 2012;25:498–507
  • Kovo M, Schreiber L, Ben-Haroush A, et al. The placental component in early-onset and late-onset preeclampsia in relation to fetal growth restriction. Prenat Diagn 2012;32:632–37
  • Stark MW, Clark L, Craver RD. Histologic differences in placentas of preeclamptic/eclamptic gestations by birthweight, placental weight, and time of onset. Pediatr Dev Pathol 2014;17:181–9
  • Kovo M, Schreiber L, Bar J. Placental vascular pathology as a mechanism of disease in pregnancy complications. Thromb Res 2013;131:S18–21
  • Chaiworapongsa T, Chaemsaithong P, Yeo L, et al. Pre-eclampsia part 1: current understanding of its pathophysiology. Nat Rev Nephrol 2014;10:466–80
  • Aviram R, T BS, Kidron D. Placental aetiologies of foetal growth restriction: clinical and pathological differences. Early Hum Dev 2010;86:59–63
  • Spinillo A, Gardella B, Bariselli S, et al. Placental histopathological correlates of umbilical artery Doppler velocimetry in pregnancies complicated by fetal growth restriction. Prenat Diagn 2012;32:1263–72
  • Parra-Saavedra M, Crovetto F, Triunfo S, et al. Placental findings in late-onset SGA births without Doppler signs of placental insufficiency. Placenta 2013;34:1136–41
  • Triunfo S, Lobmaier S, Parra-Saavedra M, et al. Angiogenic factors at diagnosis of late-onset small-for-gestational age and histological placental underperfusion. Placenta 2014;35:398–403
  • Parra-Saavedra M, Crovetto F, Triunfo S, et al. Association of Doppler parameters with placental signs of underperfusion in late-onset SGA pregnancies. Ultrasound Obstet Gynecol 2014;44:330–7
  • Ball E, Bulmer JN, Ayis S, et al. Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion. J Pathol 2006;208:535–42
  • 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;30:700–4
  • Dommisse J, Tiltman AJ. Placental bed biopsies in placental abruption. Br J Obstet Gynaecol 1992;99:651–54
  • Ananth CV, Peltier MR, Kinzler WL, et al. Chronic hypertension and risk of placental abruption: is the association modified by ischemic placental disease? Am J Obstet Gynecol 2007;197:273 e271–77
  • Arias F, Rodriquez L, Rayne SC, et al. Maternal placental vasculopathy and infection: two distinct subgroups among patients with preterm labor and preterm ruptured membranes. Am J Obstet Gynecol 1993;168:585–91
  • Kim YM, Bujold E, Chaiworapongsa T, et al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2003;189:1063–69
  • Romero R, Espinoza J, Kusanovic JP, et al. The preterm parturition syndrome. BJOG. 2006;113:17–42
  • Chaiworapongsa T, Romero R, Tarca A, et al. A subset of patients destined to develop spontaneous preterm labor has an abnormal angiogenic/anti-angiogenic profile in maternal plasma: evidence in support of pathophysiologic heterogeneity of preterm labor derived from a longitudinal study. J Matern Fetal Neonatal Med 2009;22:1122–39
  • Roescher AM, Hitzert MM, Timmer A, et al. Placental pathology is associated with illness severity in preterm infants in the first twenty-four hours after birth. Early Hum Dev 2011;87:315–19
  • Kovo M, Schreiber L, Ben-Haroush A, et al. The placental factor in spontaneous preterm labor with and without premature rupture of membranes. J Perinat Med 2011;39:423–29
  • Roescher AM, Timmer A, Hitzert MM, et al. Placental pathology and neurological morbidity in preterm infants during the first two weeks after birth. Early Hum Dev 2014;90:21–25
  • Kim YM, Chaiworapongsa T, Gomez R, et al. Failure of physiologic transformation of the spiral arteries in the placental bed in preterm premature rupture of membranes. Am J Obstet Gynecol 2002;187:1137–42
  • Arias F, Victoria A, Cho K, et al. Placental histology and clinical characteristics of patients with preterm premature rupture of membranes. Obstet Gynecol 1997;89:265–71
  • Khong TY, Liddell HS, Robertson WB. Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol 1987;94:649–55
  • Clewell WH, Manchester DK. Recurrent maternal floor infarction: a preventable cause of fetal death. Am J Obstet Gynecol 1983;147:346–47
  • Nickel RE. Maternal floor infarction: an unusual cause of intrauterine growth retardation. Am J Dis Child 1988;142:1270–71
  • Andres RL, Kuyper W, Resnik R, et al. The association of maternal floor infarction of the placenta with adverse perinatal outcome. Am J Obstet Gynecol 1990;163:935–38
  • Gersell DJ. Chronic villitis, chronic chorioamnionitis, and maternal floor infarction. Semin Diagn Pathol 1993;10:251–66
  • Mandsager NT, Bendon R, Mostello D, et al. Maternal floor infarction of the placenta: prenatal diagnosis and clinical significance. Obstet Gynecol 1994;83:750–54
  • Bendon RW, Hommel AB. Maternal floor infarction in autoimmune disease: two cases. Pediatr Pathol Lab Med 1996;16:293–97
  • Katz J, Street A, Arias I. Individual differences in self-appraisals and responses to dating violence scenarios. Violence Vict 1997;12:265–76
  • Katzman PJ, Genest DR. Maternal floor infarction and massive perivillous fibrin deposition: histological definitions, association with intrauterine fetal growth restriction, and risk of recurrence. Pediatr Dev Pathol 2002;5:159–64
  • Sebire NJ, Backos M, Goldin RD, et al. Placental massive perivillous fibrin deposition associated with antiphospholipid antibody syndrome. BJOG 2002;109:570–73
  • Bane AL, Gillan JE. Massive perivillous fibrinoid causing recurrent placental failure. BJOG 2003;110:292–95
  • Gupta N, Sebire NJ, Miskry T, et al. Massive perivillous fibrin deposition associated with discordant fetal growth in a dichorionic twin pregnancy. J Obstet Gynaecol 2004;24:579–80
  • Romero R, Whitten A, Korzeniewski SJ, et al. Maternal floor infarction/massive perivillous fibrin deposition: a manifestation of maternal antifetal rejection? Am J Reprod Immunol 2013;70:285–98
  • Whitten AE, Romero R, Korzeniewski SJ, et al. Evidence of an imbalance of angiogenic/antiangiogenic factors in massive perivillous fibrin deposition (maternal floor infarction): a placental lesion associated with recurrent miscarriage and fetal death. Am J Obstet Gynecol 2013;208:310 e311–310 e311
  • Al-Sahan N, Grynspan D, von Dadelszen P, et al. Maternal floor infarction: management of an underrecognized pathology. J Obstet Gynaecol Res 2014;40:293–96
  • Dempster WJ, Harrison CV, Shackman R. Rejection processes in human homotransplanted kidneys. Br Med J 1964;2:969–76
  • Hess ML, Hastillo A, Mohanakumar T, et al. Accelerated atherosclerosis in cardiac transplantation: role of cytotoxic B-cell antibodies and hyperlipidemia. Circulation 1983;68:II94–101
  • Palmer DC, Tsai CC, Roodman ST, et al. Heart graft arteriosclerosis. An ominous finding on endomyocardial biopsy. Transplantation 1985;39:385–88
  • Mitchell RN, Libby P. Vascular remodeling in transplant vasculopathy. Circ Res 2007;100:967–78
  • Biedermann BC. Vascular endothelium and graft-versus-host disease. Best Pract Res Clin Haematol 2008;21:129–38
  • Mitchell RN. Graft vascular disease: immune response meets the vessel wall. Annu Rev Pathol 2009;4:19–47
  • Pareja E, Cortes M, Navarro R, et al. Vascular complications after orthotopic liver transplantation: hepatic artery thrombosis. Transplant Proc 2010;42:2970–72
  • Torzewski J, Bowyer DE, Waltenberger J, et al. Processes in atherogenesis: complement activation. Atherosclerosis 1997;132:131–8
  • Niculescu F, Rus H. The role of complement activation in atherosclerosis. Immunol Res 2004;30:73–80
  • Haskard DO, Boyle JJ, Mason JC. The role of complement in atherosclerosis. Curr Opin Lipidol 2008;19:478–82
  • Shields KJ, Stolz D, Watkins SC, et al. Complement proteins C3 and C4 bind to collagen and elastin in the vascular wall: a potential role in vascular stiffness and atherosclerosis. Clin Transl Sci 2011;4:146–52
  • Hertle E, van Greevenbroek MM, Arts IC, et al. Distinct associations of complement C3a and its precursor C3 with atherosclerosis and cardiovascular disease. The CODAM study. Thromb Haemost 2014;111:1102–11
  • Kitzmiller JL, Benirschke K. Immunofluorescent study of placental bed vessels in pre-eclampsia of pregnancy. Am J Obstet Gynecol 1973;115:248–51
  • Weir PE. Immunofluorescent studies of the uteroplacental arteries in normal pregnancy. Br J Obstet Gynaecol 1981;88:301–7
  • Labarrere CA, Althabe OH. Primary chronic abortion, preeclampsia, idiopathic intrauterine growth retardation, hydatidiform mole, and choriocarcinoma: a unifying concept. Am J Reprod Immunol Microbiol 1986;10:156–57
  • Bulmer JN. Immune aspects of pathology of the placental bed contributing to pregnancy pathology. Baillieres Clin Obstet Gynaecol 1992;6:461–88
  • Lee J, Kim JS, Park JW, et al. Chronic chorioamnionitis is the most common placental lesion in late preterm birth. Placenta 2013;34:681–89
  • Lee J, Romero R, Xu Y, et al. Maternal HLA panel-reactive antibodies in early gestation positively correlate with chronic chorioamnionitis: evidence in support of the chronic nature of maternal anti-fetal rejection. Am J Reprod Immunol 2011;66:510–26
  • Lee J, Romero R, Xu Y, et al. A signature of maternal anti-fetal rejection in spontaneous preterm birth: chronic chorioamnionitis, anti-human leukocyte antigen antibodies, and C4d. PLoS One 2011;6:e16806
  • Katabuchi H, Yih S, Ohba T, et al. Characterization of macrophages in the decidual atherotic spiral artery with special reference to the cytology of foam cells. Med Electron Microsc 2003;36:253–62
  • Libby P. Inflammation in atherosclerosis. Nature 2002;420:868–74
  • Libby P. Atherosclerosis: disease biology affecting the coronary vasculature. Am J Cardiol 2006;98:3Q–9Q
  • Rocha VZ, Libby P. Obesity, inflammation, and atherosclerosis. Nat Rev Cardiol 2009;6:399–409
  • Libby P, Ridker PM, Hansson GK. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol 2009;54:2129–38
  • Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol 2009;27:165–97
  • Packard RR, Lichtman AH, Libby P. Innate and adaptive immunity in atherosclerosis. Semin Immunopathol 2009;31:5–22
  • Andersson J, Libby P, Hansson GK. Adaptive immunity and atherosclerosis. Clin Immunol 2010;134:33–46
  • Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 2011;473:317–25
  • Legein B, Temmerman L, Biessen EA, et al. Inflammation and immune system interactions in atherosclerosis. Cell Mol Life Sci 2013;70:3847–69
  • Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 2013;38:1092–104
  • Rosenfeld ME. Inflammation and atherosclerosis: direct versus indirect mechanisms. Curr Opin Pharmacol 2013;13:154–60
  • Woollard KJ. Immunological aspects of atherosclerosis. Clin Sci (Lond) 2013;125:221–35
  • Ait-Oufella H, Sage AP, Mallat Z, et al. Adaptive (T and B cells) immunity and control by dendritic cells in atherosclerosis. Circ Res 2014;114:1640–60
  • Mach F, Sauty A, Iarossi AS, et al. Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J Clin Invest 1999;104:1041–50
  • Xu Y, Tarquini F, Romero R, et al. Peripheral CD300a+CD8+ T lymphocytes with a distinct cytotoxic molecular signature increase in pregnant women with chronic chorioamnionitis. Am J Reprod Immunol 2012;67:184–97
  • Salafia CM, Pezzullo JC, Lopez-Zeno JA, et al. Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 1995;173:1097–105
  • Kupferminc MJ, Eldor A, Steinman N, et al. Increased frequency of genetic thrombophilia in women with complications of pregnancy. N Engl J Med 1999;340:9–13
  • Chaiworapongsa T, Yoshimatsu J, Espinoza J, et al. Evidence of in vivo generation of thrombin in patients with small-for-gestational-age fetuses and pre-eclampsia. J Matern Fetal Neonatal Med 2002;11:362–67
  • Agorastos T, Karavida A, Lambropoulos A, et al. Factor V Leiden and prothrombin G20210A mutations in pregnancies with adverse outcome. J Matern Fetal Neonatal Med 2002;12:267–73
  • Brenner B, Kupferminc MJ. Inherited thrombophilia and poor pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 2003;17:427–39
  • Kupferminc JM. Management of thrombophilia in women with PVC. Thromb Res 2005;115:46–50
  • Erez O, Hoppensteadt D, Romero R, et al. Preeclampsia is associated with low concentrations of protein Z. J Matern Fetal Neonatal Med 2007;20:661–67
  • Erez O, Romero R, Kim SS, et al. Over-expression of the thrombin receptor (PAR-1) in the placenta in preeclampsia: a mechanism for the intersection of coagulation and inflammation. J Matern Fetal Neonatal Med 2008;21:345–55
  • Kupferminc MJ, Rimon E, Many A, et al. Low molecular weight heparin treatment during subsequent pregnancies of women with inherited thrombophilia and previous severe pregnancy complications. J Matern Fetal Neonatal Med 2011;24:1042–45
  • Conserva V, Muggiasca M, Arrigoni L, et al. Recurrence and severity of abnormal pregnancy outcome in patients treated by low-molecular-weight heparin: a prospective pilot study. J Matern Fetal Neonatal Med 2012;25:1467–73
  • Kusanovic JP, Espinoza J, Romero R, et al. Plasma protein Z concentrations in pregnant women with idiopathic intrauterine bleeding and in women with spontaneous preterm labor. J Matern Fetal Neonatal Med 2007;20:453–63
  • Erez O, Romer R, Vaisbuch E, et al. Changes in amniotic fluid concentration of thrombin-antithrombin III complexes in patients with preterm labor: evidence of an increased thrombin generation. J Matern Fetal Neonatal Med 2009;22:971–82
  • Kramer MS, Kahn SR, Rozen R, et al. Vasculopathic and thrombophilic risk factors for spontaneous preterm birth. Int J Epidemiol 2009;38:715–23
  • Erez O, Espinoza J, Chaiworapongsa T, et al. A link between a hemostatic disorder and preterm PROM: a role for tissue factor and tissue factor pathway inhibitor. J Matern Fetal Neonatal Med 2008;21:732–44
  • Gargano JW, Holzman CB, Senagore PK, et al. Polymorphisms in thrombophilia and renin-angiotensin system pathways, preterm delivery, and evidence of placental hemorrhage. Am J Obstet Gynecol 2009;201:317 e311–19
  • Erez O, Romero R, Vaisbuch E, et al. High tissue factor activity and low tissue factor pathway inhibitor concentrations in patients with preterm labor. J Matern Fetal Neonatal Med 2010;23:23–33
  • Alonso A, Soto I, Urgelles MF, et al. Acquired and inherited thrombophilia in women with unexplained fetal losses. Am J Obstet Gynecol 2002;187:1337–42
  • Robertson L, Wu O, Langhorne P, et al. Thrombophilia in pregnancy: a systematic review. Br J Haematol 2006;132:171–96
  • Erez O, Gotsch F, Mazaki-Tovi S, et al. Evidence of maternal platelet activation, excessive thrombin generation, and high amniotic fluid tissue factor immunoreactivity and functional activity in patients with fetal death. J Matern Fetal Neonatal Med 2009;22:672–87
  • Benedetto C, Marozio L, Tavella AM, et al. Coagulation disorders in pregnancy: acquired and inherited thrombophilias. Ann N Y Acad Sci 2010;1205:106–17
  • Kjellberg U, van Rooijen M, Bremme K, et al. Factor V Leiden mutation and pregnancy-related complications. Am J Obstet Gynecol 2010;203:469 e461–8
  • Werner EF, Lockwood CJ. Thrombophilias and stillbirth. Clin Obstet Gynecol 2010;53:617–27
  • Aracic N, Roje D, Drmic Hofman I, et al. Low molecular weight heparin treatment and impact of inherited thrombophilia type in pregnancies with previous adverse outcome. J Matern Fetal Neonatal Med 2014;22:1–5. [Epub ahead of print]
  • Arias F, Romero R, Joist H, et al. Thrombophilia: a mechanism of disease in women with adverse pregnancy outcome and thrombotic lesions in the placenta. J Matern Fetal Med 1998;7:277–86
  • Vern TZ, Alles AJ, Kowal-Vern A, et al. Frequency of factor V(Leiden) and prothrombin G20210A in placentas and their relationship with placental lesions. Hum Pathol 2000;31:1036–43
  • Ariel I, Anteby E, Hamani Y, et al. Placental pathology in fetal thrombophilia. Hum Pathol 2004;35:729–33
  • Redline RW, Ariel I, Baergen RN, et al. Fetal vascular obstructive lesions: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2004;7:443–52
  • Saleemuddin A, Tantbirojn P, Sirois K, et al. Obstetric and perinatal complications in placentas with fetal thrombotic vasculopathy. Pediatr Dev Pathol 2010;13:459–64
  • Lepais L, Gaillot-Durand L, Boutitie F, et al. Fetal thrombotic vasculopathy is associated with thromboembolic events and adverse perinatal outcome but not with neurologic complications: a retrospective cohort study of 54 cases with a 3-year follow-up of children. Placenta 2014;35:611–17
  • Fox H, Langley FA. Leukocytic infiltration of the placenta and umbilical cord. A clinico-pathologic study. Obstet Gynecol 1971;37:451–58
  • Dong Y, St Clair PJ, Ramzy I, et al. A microbiologic and clinical study of placental inflammation at term. Obstet Gynecol 1987;70:175–82
  • Moller GH, Woods DL, Malan AF, et al. Chorio-amnionitis in relation to mode of delivery at term. S Afr Med J 1989;76:201–2
  • Nordenvall M, Sandstedt B. Chorioamnionitis in relation to gestational outcome in a Swedish population. Eur J Obstet Gynecol Reprod Biol 1990;36:59–67
  • Halgunset J, Johnsen H, Kjollesdal AM, et al. Cytokine levels in amniotic fluid and inflammatory changes in the placenta from normal deliveries at term. Eur J Obstet Gynecol Reprod Biol 1994;56:153–60
  • Keski-Nisula L, Aalto ML, Katila ML, et al. Intrauterine inflammation at term: a histopathologic study. Hum Pathol 2000;31:841–46
  • Hebisch G, Grauaug AA, Neumaier-Wagner PM, et al. The relationship between cervical dilatation, interleukin-6 and interleukin-8 during term labor. Acta Obstet Gynecol Scand 2001;80:840–48
  • Lee SE, Romero R, Kim CJ, et al. Funisitis in term pregnancy is associated with microbial invasion of the amniotic cavity and intra-amniotic inflammation. J Matern Fetal Neonatal Med 2006;19:693–97
  • Chaiworapongsa T, Erez O, Kusanovic JP, et al. Amniotic fluid heat shock protein 70 concentration in histologic chorioamnionitis, term and preterm parturition. J Matern Fetal Neonatal Med 2008;21:449–61
  • Seong HS, Lee SE, Kang JH, et al. The frequency of microbial invasion of the amniotic cavity and histologic chorioamnionitis in women at term with intact membranes in the presence or absence of labor. Am J Obstet Gynecol 2008;199:375 e371–75
  • Gotsch F, Romero R, Kusanovic JP, et al. The anti-inflammatory limb of the immune response in preterm labor, intra-amniotic infection/inflammation, and spontaneous parturition at term: a role for interleukin-10. J Matern Fetal Neonatal Med 2008;21:529–47
  • Hamill N, Romero R, Gotsch F, et al. Exodus-1 (CCL20): evidence for the participation of this chemokine in spontaneous labor at term, preterm labor, and intrauterine infection. J Perinat Med 2008;36:217–27
  • Gotsch F, Romero R, Chaiworapongsa T, et al. Evidence of the involvement of caspase-1 under physiologic and pathologic cellular stress during human pregnancy: a link between the inflammasome and parturition. J Matern Fetal Neonatal Med 2008;21:605–16
  • Lee SM, Romero R, Lee KA, et al. The frequency and risk factors of funisitis and histologic chorioamnionitis in pregnant women at term who delivered after the spontaneous onset of labor. J Matern Fetal Neonatal Med 2011;24:37–42
  • Lee SM, Lee KA, Kim SM, et al. The risk of intra-amniotic infection, inflammation and histologic chorioamnionitis in term pregnant women with intact membranes and labor. Placenta 2011;32:516–21

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