Semin Liver Dis 2008; 28(3): 315-327
DOI: 10.1055/s-0028-1085099
© Thieme Medical Publishers

Hepatic Vascular Involvement Related to Pregnancy, Oral Contraceptives, and Estrogen Replacement Therapy

Jean-Marc Perarnau1 , Yannick Bacq1
  • 1Service d'Hépatogastroentérologie, Hôpital Trousseau, Tours, France
Further Information

Publication History

Publication Date:
23 September 2008 (online)

ABSTRACT

Both pregnancy and oral contraception (mainly when estrogen is included) may precipitate the development of Budd–Chiari syndrome in patients with underlying thrombophilia. By contrast, there is little evidence for such a role of pregnancy and oral contraception in women with portal vein thrombosis. In pregnant women, special modalities for anticoagulation are required, whereas the management of portal hypertension can be similar to that recommended in other diseases and settings. Hereditary hemorrhagic telangiectasia may deteriorate during pregnancy and improve after delivery. Hepatic sinusoidal dilatation and hepatic peliosis are classic complications of long-term use of oral contraceptives. The impact of pregnancy or oral contraceptives on the natural history on hemangioma and focal nodular hyperplasia appears to be limited. Preeclampsia, a liver disease unique to pregnancy, may be complicated by life-threatening liver vascular involvement, especially when the syndrome of hemolysis, elevated liver enzymes, and low platelet count (HELLP syndrome) is present.

REFERENCES

  • 1 Lund C J, Donovan J C. Blood volume during pregnancy. Significance of plasma and red cell volumes.  Am J Obstet Gynecol. 1967;  98 394-403
  • 2 Peck T M, Arias F. Hematologic changes associated with pregnancy.  Clin Obstet Gynecol. 1979;  22 785-798
  • 3 Rovinsky J J, Jaffin H. Cardiovascular hemodynamics in pregnancy. 3. Cardiac rate, stroke volume, total peripheral resistance, and central blood volume in multiple pregnancy. Synthesis of results.  Am J Obstet Gynecol. 1966;  95 787-794
  • 4 Laakso L, Ruotsalainen P, Punnonen R, Maatela J. Hepatic blood flow during late pregnancy.  Acta Obstet Gynecol Scand. 1971;  50 175-178
  • 5 Munnell E W, Taylor H C. Liver blood flow in pregnancy-hepatic vein catheterization.  J Clin Invest. 1947;  26 952-956
  • 6 Clapp III J F, Stepanchak W, Tomaselli J, Kortan M, Faneslow S. Portal vein blood flow-effects of pregnancy, gravity, and exercise.  Am J Obstet Gynecol. 2000;  183 167-172
  • 7 Mayo M A, Lopez-Cano A, Mendez C et al.. Hemodynamic modifications in splenic circulation studied by echo-Doppler during pregnancy.  Gastroenterol Hepatol. 2002;  25 148-152
  • 8 James A H. Prevention and management of venous thromboembolism in pregnancy.  Am J Med. 2007;  120 S26-S34
  • 9 Heit J A, Kobbervig C E, James A H et al.. Trends in the incidence of venous thromboembolism during pregnancy or postpartum: a 30-year population-based study.  Ann Intern Med. 2005;  143 697-706
  • 10 Lim W, Eikelboom J W, Ginsberg J S. Inherited thrombophilia and pregnancy associated venous thromboembolism.  BMJ. 2007;  334 1318-1321
  • 11 Battaglioli T, Martinelli I. Hormone therapy and thromboembolic disease.  Curr Opin Hematol. 2007;  14 488-493
  • 12 Rosing J, Middeldorp S, Curvers J et al.. Low-dose oral contraceptives and acquired resistance to activated protein C: a randomised cross-over study.  Lancet. 1999;  354 2036-2040
  • 13 Cole J A, Norman H, Doherty M, Walker A M. Venous thromboembolism, myocardial infarction, and stroke among transdermal contraceptive system users.  Obstet Gynecol. 2007;  109 339-346
  • 14 Wu O, Robertson L, Langhorne P et al.. Oral contraceptives, hormone replacement therapy, thrombophilias and risk of venous thromboembolism: a systematic review. The Thrombosis Risk and Economic Assessment of Thrombophilia Screening (TREATS) Study.  Thromb Haemost. 2005;  94 17-25
  • 15 Wu O, Robertson L, Twaddle S et al.. Screening for thrombophilia in high-risk situations: a meta-analysis and cost-effectiveness analysis.  Br J Haematol. 2005;  131 80-90
  • 16 Canonico M, Oger E, Plu-Bureau G et al.. Hormone therapy and venous thromboembolism among postmenopausal women: impact of the route of estrogen administration and progestogens: the ESTHER study.  Circulation. 2007;  115 840-845
  • 17 Toorians A W, Thomassen M C, Zweegman S et al.. Venous thrombosis and changes of hemostatic variables during cross-sex hormone treatment in transsexual people.  J Clin Endocrinol Metab. 2003;  88 5723-5729
  • 18 Miller A P, Chen Y F, Xing D, Feng W, Oparil S. Hormone replacement therapy and inflammation: interactions in cardiovascular disease.  Hypertension. 2003;  42 657-663
  • 19 Sgarabotto M, Baldini M, Dei Cas A et al.. Effects of raloxifene and continuous combined hormone therapy on haemostasis variables: a multicenter, randomized, double-blind study.  Thromb Res. 2007;  119 85-91
  • 20 Kluft C. Effects of hormone treatment on hemostasis variables.  Climacteric. 2007;  10(Suppl 2) 32-37
  • 21 de Franchis R. Evolving consensus in portal hypertension. Report of the Baveno IV Consensus Workshop on Methodology of Diagnosis and Therapy in Portal Hypertension.  J Hepatol. 2005;  43 167-176
  • 22 Plessier A, Sibert A, Consigny Y et al.. Aiming at minimal invasiveness as a therapeutic strategy for Budd-Chiari syndrome.  Hepatology. 2006;  44 1308-1316
  • 23 Rautou P E, Angermayr B, Raffa S et al.. Maternal and fetal outcome in 27 women with Budd-Chiari syndrome (BCS) and 41 pregnancies.  Hepatology. 2007;  46 563 , (abstract)
  • 24 Marks P W. Management of thromboembolism in pregnancy.  Semin Perinatol. 2007;  31 227-231
  • 25 Khuroo M S, Datta D V. Budd-Chiari syndrome following pregnancy. Report of 16 cases, with roentgenologic, hemodynamic and histologic studies of the hepatic outflow tract.  Am J Med. 1980;  68 113-121
  • 26 Singh V, Sinha S K, Nain C K et al.. Budd-Chiari syndrome: our experience of 71 patients.  J Gastroenterol Hepatol. 2000;  15 550-554
  • 27 Dilawari J B, Bambery P, Chawla Y et al.. Hepatic outflow obstruction (Budd-Chiari syndrome). Experience with 177 patients and a review of the literature.  Medicine (Baltimore). 1994;  73 21-36
  • 28 Mohanty D, Shetty S, Ghosh K, Pawar A, Abraham P. Hereditary thrombophilia as a cause of Budd-Chiari syndrome: a study from Western India.  Hepatology. 2001;  34 666-670
  • 29 Denninger M H, Chait Y, Casadevall N et al.. Cause of portal or hepatic venous thrombosis in adults: the role of multiple concurrent factors.  Hepatology. 2000;  31 587-591
  • 30 Webb J A, Thomsen H S, Morcos S K. The use of iodinated and gadolinium contrast media during pregnancy and lactation.  Eur Radiol. 2005;  15 1234-1240
  • 31 Lin S P, Brown J J. MR contrast agents: physical and pharmacologic basics.  J Magn Reson Imaging. 2007;  25 884-899
  • 32 Joffe G M, Aisenbrey G A, Argubright K F. Budd-Chiari syndrome, systemic lupus erythematosus, and secondary antiphospholipid antibody syndrome in pregnancy.  Obstet Gynecol. 2005;  106 1191-1194
  • 33 Wildberger J E, Vorwerk D, Winograd R et al.. New TIPS placement in pregnancy in recurrent esophageal varices hemorrhage–assessment of fetal radiation exposure.  Rofo. 1998;  169 429-431
  • 34 Savage C, Patel J, Lepe M R, Lazarre C H, Rees C R. Transjugular intrahepatic portosystemic shunt creation for recurrent gastrointestinal bleeding during pregnancy.  J Vasc Interv Radiol. 2007;  18 902-904
  • 35 Valla D C. Hepatic vein thrombosis (Budd-Chiari syndrome).  Semin Liver Dis. 2002;  22 5-14
  • 36 Janssen H L, Meinardi J R, Vleggaar F P et al.. Factor V Leiden mutation, prothrombin gene mutation, and deficiencies in coagulation inhibitors associated with Budd-Chiari syndrome and portal vein thrombosis: results of a case-control study.  Blood. 2000;  96 2364-2368
  • 37 Pajor A, Lehoczky D. Pregnancy and extrahepatic portal hypertension. Review and report on the management.  Gynecol Obstet Invest. 1990;  30 193-197
  • 38 Cheng Y S. Pregnancy in liver cirrhosis and/or portal hypertension.  Am J Obstet Gynecol. 1977;  128 812-822
  • 39 Kochhar R, Kumar S, Goel R C et al.. Pregnancy and its outcome in patients with noncirrhotic portal hypertension.  Dig Dis Sci. 1999;  44 1356-1361
  • 40 Garcia-Tsao G, Sanyal A J, Grace N D, Carey W. Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis.  Hepatology. 2007;  46 922-938
  • 41 Mahadevan U, Kane S. American Gastroenterological Association institute technical review on the use of gastrointestinal medications in pregnancy.  Gastroenterology. 2006;  131 283-311
  • 42 Starkel P, Horsmans Y, Geubel A. Endoscopic band ligation: a safe technique to control bleeding esophageal varices in pregnancy.  Gastrointest Endosc. 1998;  48 212-214
  • 43 Hay J E. Liver disease in pregnancy.  Hepatology. 2008;  47 1067-1076
  • 44 Aggarwal N, Sawhney H, Vasishta K, Dhiman R K, Chawla Y. Non-cirrhotic portal hypertension in pregnancy.  Int J Gynaecol Obstet. 2001;  72 1-7
  • 45 Britton R C. Pregnancy and esophageal varices.  Am J Surg. 1982;  143 421-425
  • 46 Restaino A, Campobasso C, D'Aloya A et al.. Cirrhosis and pregnancy. A case report and review of the literature.  Clin Exp Obstet Gynecol. 1996;  23 240-247
  • 47 Heriot J A, Steven C M, Sattin R S. Elective forceps delivery and extradural anaesthesia in a primigravida with portal hypertension and oesophageal varices.  Br J Anaesth. 1996;  76 325-327
  • 48 Sarin S K, Sollano J D, Chawla Y K et al.. Consensus on extra-hepatic portal vein obstruction.  Liver Int. 2006;  26 512-519
  • 49 Goodrich M A, James E M, Baldus W P, Lomboy C T, Harms R W. Portal vein thrombosis associated with pregnancy. A case report.  J Reprod Med. 1993;  38 969-972
  • 50 Janssen H L, Wijnhoud A, Haagsma E B et al.. Extrahepatic portal vein thrombosis: aetiology and determinants of survival.  Gut. 2001;  49 720-724
  • 51 Primignani M, Martinelli I, Bucciarelli P et al.. Risk factors for thrombophilia in extrahepatic portal vein obstruction.  Hepatology. 2005;  41 603-608
  • 52 Yapar E G, Bilge U, Dumanli H, Vural T, Gokmen O. Portal vein thrombosis concomitant with thrombophilia during pregnancy.  Eur J Obstet Gynecol Reprod Biol. 1996;  68 213-217
  • 53 Bianconcini G, Parolari G, Gobbi F, Zinelli G. Pregnancy complication in homozygous (delta beta) zero-thalassemia. A clinical case.  Minerva Med. 1993;  84 203-209
  • 54 Condat B, Pessione F, Helene Denninger M, Hillaire S, Valla D. Recent portal or mesenteric venous thrombosis: increased recognition and frequent recanalization on anticoagulant therapy.  Hepatology. 2000;  32 466-470
  • 55 Valla D C, Condat B. Portal vein thrombosis in adults: pathophysiology, pathogenesis and management.  J Hepatol. 2000;  32 865-871
  • 56 DeLeve L D, Shulman H M, McDonald G B. Toxic injury to hepatic sinusoids: sinusoidal obstruction syndrome (veno-occlusive disease).  Semin Liver Dis. 2002;  22 27-42
  • 57 Hagglund H, Remberger M, Klaesson S et al.. Norethisterone treatment, a major risk-factor for veno-occlusive disease in the liver after allogeneic bone marrow transplantation.  Blood. 1998;  92 4568-4572
  • 58 Hillaire S, Bonte E, Denninger M H et al.. Idiopathic non-cirrhotic intrahepatic portal hypertension in the West: a re-evaluation in 28 patients.  Gut. 2002;  51 275-280
  • 59 Garcia-Tsao G. Liver involvement in hereditary hemorrhagic telangiectasia (HHT).  J Hepatol. 2007;  46 499-507
  • 60 Shovlin C L, Winstock A R, Peters A M, Jackson J E, Hughes J M. Medical complications of pregnancy in hereditary haemorrhagic telangiectasia.  QJM. 1995;  88 879-887
  • 61 Livneh A, Langevitz P, Morag B, Catania A, Pras M. Functionally reversible hepatic arteriovenous fistulas during pregnancy in patients with hereditary hemorrhagic telangiectasia.  South Med J. 1988;  81 1047-1049
  • 62 Hillert C, Broering D C, Gundlach M et al.. Hepatic involvement in hereditary hemorrhagic telangiectasia: an unusual indication for liver transplantation.  Liver Transpl. 2001;  7 266-268
  • 63 McInroy B, Zajko A B, Pinna A D. Biliary necrosis due to hepatic involvement with hereditary hemorrhagic telangiectasia.  AJR Am J Roentgenol. 1998;  170 413-415
  • 64 Reddy K R, Kligerman S, Levi J et al.. Benign and solid tumors of the liver: relationship to sex, age, size of tumors, and outcome.  Am Surg. 2001;  67 173-178
  • 65 Saegusa T, Ito K, Oba N et al.. Enlargement of multiple cavernous hemangioma of the liver in association with pregnancy.  Intern Med. 1995;  34 207-211
  • 66 Gungor T, Aytan H, Tapisiz O L, Zergeroglu S. An unusual case of incidental rupture of liver hemangioma during labor.  Chin Med J (Engl). 2004;  117 311-313
  • 67 Krasuski P, Poniecka A, Gal E, Wali A. Intrapartum spontaneous rupture of liver hemangioma.  J Matern Fetal Med. 2001;  10 290-292
  • 68 Fouchard I, Rosenau L, Cales P, Allory P. Survenue d'hémangiomes hépatiques au cours de la grossesse.  Gastroenterol Clin Biol. 1994;  18 512-515
  • 69 Reyes M, Monsalve V, Hepp J, Vaccaro H. A giant hepatic hemangioma and pregnancy.  Rev Chil Obstet Ginecol. 1992;  57 359-361
  • 70 Graham E, Cohen A W, Soulen M, Faye R. Symptomatic liver hemangioma with intra-tumor hemorrhage treated by angiography and embolization during pregnancy.  Obstet Gynecol. 1993;  81 813-816
  • 71 Glinkova V, Shevah O, Boaz M, Levine A, Shirin H. Hepatic haemangiomas: possible association with female sex hormones.  Gut. 2004;  53 1352-1355
  • 72 Gemer O, Moscovici O, Ben-Horin C L et al.. Oral contraceptives and liver hemangioma: a case-control study.  Acta Obstet Gynecol Scand. 2004;  83 1199-1201
  • 73 Ozakyol A, Kebapci M. Enhanced growth of hepatic hemangiomatosis in two adults after postmenopausal estrogen replacement therapy.  Tohoku J Exp Med. 2006;  210 257-261
  • 74 Lui W, Zhang S, Hu T et al.. Sex hormone receptors of hemangiomas in children.  Chin Med J (Engl). 1997;  110 349-351
  • 75 Xiao X, Hong L, Sheng M. Promoting effect of estrogen on the proliferation of hemangioma vascular endothelial cells in vitro.  J Pediatr Surg. 1999;  34 1603-1605
  • 76 Xiao X, Liu J, Sheng M. Synergistic effect of estrogen and VEGF on the proliferation of hemangioma vascular endothelial cells.  J Pediatr Surg. 2004;  39 1107-1110
  • 77 Wanless I R. Vasular disorders. In: MacSween RNM, Burt AD, Portman BC, Ishak KG, Scheuer PJ, Anthony PP Pathology of the Liver. 4th ed. Glasgow, UK; Churchill Livingstone 2002: 540-573
  • 78 Cobey F C, Salem R R. A review of liver masses in pregnancy and a proposed algorithm for their diagnosis and management.  Am J Surg. 2004;  187 181-191
  • 79 Scott L D, Katz A R, Duke J H, Cowan D F, Maklad N F. Oral contraceptives, pregnancy, and focal nodular hyperplasia of the liver.  JAMA. 1984;  251 1461-1463
  • 80 Heinemann L A, Weimann A, Gerken G et al.. Modern oral contraceptive use and benign liver tumors: the German Benign Liver Tumor Case-Control Study.  Eur J Contracept Reprod Health Care. 1998;  3 194-200
  • 81 Scalori A, Tavani A, Gallus S, La Vecchia C, Colombo M. Oral contraceptives and the risk of focal nodular hyperplasia of the liver: a case-control study.  Am J Obstet Gynecol. 2002;  186 195-197
  • 82 Mathieu D, Kobeiter H, Maison P et al.. Oral contraceptive use and focal nodular hyperplasia of the liver.  Gastroenterology. 2000;  118 560-564
  • 83 Spellberg M A, Mirro J, Chowdhury L. Hepatic sinusoidal dilatation related to oral contraceptives. A study of two patients showing ultrastructural changes.  Am J Gastroenterol. 1979;  72 248-252
  • 84 Winkler K, Poulsen H. Liver disease with periportal sinusoidal dilatation. A possible complication to contraceptive steroids.  Scand J Gastroenterol. 1975;  10 699-704
  • 85 Balazs M. Sinusoidal dilatation of the liver in patients on oral contraceptives. Electron microscopical study of 14 cases.  Exp Pathol. 1988;  35 231-237
  • 86 Camilleri M, Schafler K, Chadwick V S, Hodgson H J, Weinbren K. Periportal sinusoidal dilatation, inflammatory bowel disease, and the contraceptive pill.  Gastroenterology. 1981;  80 810-815
  • 87 Raufman J P, Miller D L, Gumucio J J. Estrogen-induced zonal changes in rat liver sinusoids.  Gastroenterology. 1980;  79 1174-1177
  • 88 Oligny L L, Lough J. Hepatic sinusoidal ectasia.  Hum Pathol. 1992;  23 953-956
  • 89 Weinberger M, Garty M, Cohen M, Russo Y, Rosenfeld J B. Ultrasonography in the diagnosis and follow-up of hepatic sinusoidal dilatation.  Arch Intern Med. 1985;  145 927-929
  • 90 Fisher M R, Neiman H L. Periportal sinusoidal dilatation associated with pregnancy.  Cardiovasc Intervent Radiol. 1984;  7 299-302
  • 91 Yang D M, Jung D H, Park C H, Kim J E, Choi S J. Imaging findings of hepatic sinusoidal dilatation.  AJR Am J Roentgenol. 2004;  183 1075-1077
  • 92 Iannaccone R, Federle M P, Brancatelli G et al.. Peliosis hepatis: spectrum of imaging findings.  AJR Am J Roentgenol. 2006;  187 W43-52
  • 93 van Erpecum K J, Janssens A R, Kreuning J et al.. Generalized peliosis hepatis and cirrhosis after long-term use of oral contraceptives.  Am J Gastroenterol. 1988;  83 572-575
  • 94 Patricot L M, Dumont M, Duvernois J P, Baulieux J, Mercatello A. A case of hepatic and splenic peliosis occurring in the puerperium after normal pregnancy.  J Gynecol Obstet Biol Reprod (Paris). 1986;  15 321-326
  • 95 Barron W M. The syndrome of preeclampsia.  Gastroenterol Clin North Am. 1992;  21 851-872
  • 96 Sibai B, Dekker G, Kupferminc M. Pre-eclampsia.  Lancet. 2005;  365 785-799
  • 97 Serrano N C. Immunology and genetic of preeclampsia.  Clin Dev Immunol. 2006;  13 197-201
  • 98 Hladunewich M, Karumanchi S A, Lafayette R. Pathophysiology of the clinical manifestations of preeclampsia.  Clin J Am Soc Nephrol. 2007;  2 543-549
  • 99 Sibai B M, Hauth J, Caritis S et al.. Hypertensive disorders in twin versus singleton gestations. National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units.  Am J Obstet Gynecol. 2000;  182 938-942
  • 100 Malone F D, Kaufman G E, Chelmow D et al.. Maternal morbidity associated with triplet pregnancy.  Am J Perinatol. 1998;  15 73-77
  • 101 Sibai B M, Ramadan M K, Usta I et al.. Maternal morbidity and mortality in 442 pregnancies with hemolysis, elevated liver enzymes, and low platelets (HELLP syndrome).  Am J Obstet Gynecol. 1993;  169 1000-1006
  • 102 Esplin M S, Fausett M B, Fraser A et al.. Paternal and maternal components of the predisposition to preeclampsia.  N Engl J Med. 2001;  344 867-872
  • 103 Dizon-Townson D S, Nelson L M, Easton K, Ward K. The factor V Leiden mutation may predispose women to severe preeclampsia.  Am J Obstet Gynecol. 1996;  175 902-905
  • 104 Ward K, Hata A, Jeunemaitre X et al.. A molecular variant of angiotensinogen associated with preeclampsia.  Nat Genet. 1993;  4 59-61
  • 105 Rajkovic A, Catalano P M, Malinow M R. Elevated homocyst(e)ine levels with preeclampsia.  Obstet Gynecol. 1997;  90 168-171
  • 106 Clausen T, Slott M, Solvoll K et al.. High intake of energy, sucrose, and polyunsaturated fatty acids is associated with increased risk of preeclampsia.  Am J Obstet Gynecol. 2001;  185 451-458
  • 107 Solomon C G, Seely E W. Brief review: hypertension in pregnancy: a manifestation of the insulin resistance syndrome?.  Hypertension. 2001;  37 232-239
  • 108 Chambers J C, Fusi L, Malik I S et al.. Association of maternal endothelial dysfunction with preeclampsia.  JAMA. 2001;  285 1607-1612
  • 109 Hulstein J J, van Runnard Heimel P J, Franx A et al.. Acute activation of the endothelium results in increased levels of active von Willebrand factor in hemolysis, elevated liver enzymes and low platelets (HELLP) syndrome.  J Thromb Haemost. 2006;  4 2569-2575
  • 110 Chappell L C, Seed P T, Briley A L et al.. Effect of antioxidants on the occurrence of pre-eclampsia in women at increased risk: a randomised trial.  Lancet. 1999;  354 810-816
  • 111 Redman C W, Sargent I L. The pathogenesis of pre-eclampsia.  Gynecol Obstet Fertil. 2001;  29 518-522
  • 112 Stella C L, Sibai B M. Preeclampsia: diagnosis and management of the atypical presentation.  J Matern Fetal Neonatal Med. 2006;  19 381-386
  • 113 Rolfes D B, Ishak K G. Liver disease in toxemia of pregnancy.  Am J Gastroenterol. 1986;  81 1138-1144
  • 114 Riely C A. The liver in preeclampsia/eclampsia: the tip of the iceberg.  Am J Gastroenterol. 1986;  81 1218-1219
  • 115 Ch'ng C L, Morgan M, Hainsworth I, Kingham J G. Prospective study of liver dysfunction in pregnancy in Southwest Wales.  Gut. 2002;  51 876-880
  • 116 Arias F, Mancilla-Jimenez R. Hepatic fibrinogen deposits in pre-eclampsia. Immunofluorescent evidence.  N Engl J Med. 1976;  295 578-582
  • 117 Weinstein L. Syndrome of hemolysis, elevated liver enzymes, and low platelet count: a severe consequence of hypertension in pregnancy.  Am J Obstet Gynecol. 1982;  142 159-167
  • 118 Martin Jr J N, Rose C H, Briery C M. Understanding and managing HELLP syndrome: the integral role of aggressive glucocorticoids for mother and child.  Am J Obstet Gynecol. 2006;  195 914-934
  • 119 Audibert F, Friedman S A, Frangieh A Y, Sibai B M. Clinical utility of strict diagnostic criteria for the HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome.  Am J Obstet Gynecol. 1996;  175 460-464
  • 120 Sibai B M, Ramadan M K, Chari R S, Friedman S A. Pregnancies complicated by HELLP syndrome (hemolysis, elevated liver enzymes, and low platelets): subsequent pregnancy outcome and long-term prognosis.  Am J Obstet Gynecol. 1995;  172 125-129
  • 121 Barton J R, Riely C A, Adamec T A et al.. Hepatic histopathologic condition does not correlate with laboratory abnormalities in HELLP syndrome (hemolysis, elevated liver enzymes, and low platelet count).  Am J Obstet Gynecol. 1992;  167 1538-1543
  • 122 Barton J R, Sibai B M. Hepatic imaging in HELLP syndrome (hemolysis, elevated liver enzymes, and low platelet count).  Am J Obstet Gynecol. 1996;  174 1820-1825 discussion 1825-1827
  • 123 Nunes J O, Turner M A, Fulcher A S. Abdominal imaging features of HELLP syndrome: a 10-year retrospective review.  AJR Am J Roentgenol. 2005;  185 1205-1210
  • 124 Bacq Y. Acute fatty liver of pregnancy.  Semin Perinatol. 1998;  22 134-140
  • 125 Sibai B M. Imitators of severe preeclampsia.  Obstet Gynecol. 2007;  109 956-966
  • 126 Ibdah J A, Bennett M J, Rinaldo P et al.. A fetal fatty-acid oxidation disorder as a cause of liver disease in pregnant women.  N Engl J Med. 1999;  340 1723-1731
  • 127 Ibdah J A. Acute fatty liver of pregnancy: an update on pathogenesis and clinical implications.  World J Gastroenterol. 2006;  12 7397-7404
  • 128 den Boer M E, Ijlst L, Wijburg F A et al.. Heterozygosity for the common LCHAD mutation (1528g> C) is not a major cause of HELLP syndrome and the prevalence of the mutation in the Dutch population is low.  Pediatr Res. 2000;  48 151-154
  • 129 Mutze S, Ahillen I, Rudnik-Schoeneborn S et al.. Neither maternal nor fetal mutation (E474Q) in the alpha-subunit of the trifunctional protein is frequent in pregnancies complicated by HELLP syndrome.  J Perinat Med. 2007;  35 76-78
  • 130 Isler C M, Rinehart B K, Terrone D A et al.. Maternal mortality associated with HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome.  Am J Obstet Gynecol. 1999;  181 924-928
  • 131 Catanzarite V A, Steinberg S M, Mosley C A et al.. Severe preeclampsia with fulminant and extreme elevation of aspartate aminotransferase and lactate dehydrogenase levels: high risk for maternal death.  Am J Perinatol. 1995;  12 310-313
  • 132 Shames B D, Fernandez L A, Sollinger H W et al.. Liver transplantation for HELLP syndrome.  Liver Transpl. 2005;  11 224-228
  • 133 Zarrinpar A, Farmer D G, Ghobrial R M et al.. Liver transplantation for HELLP syndrome.  Am Surg. 2007;  73 1013-1016
  • 134 Barton J R, Sibai B M. Diagnosis and management of hemolysis, elevated liver enzymes, and low platelets syndrome.  Clin Perinatol. 2004;  31 807-833 vii
  • 135 van Runnard Heimel P J, Franx A, Schobben A F et al.. Corticosteroids, pregnancy, and HELLP syndrome: a review.  Obstet Gynecol Surv. 2005;  60 57-70 , quiz 73–54
  • 136 Krueger K J, Hoffman B J, Lee W M. Hepatic infarction associated with eclampsia.  Am J Gastroenterol. 1990;  85 588-592
  • 137 Schwartz M L, Lien J M. Spontaneous liver hematoma in pregnancy not clearly associated with preeclampsia: a case presentation and literature review.  Am J Obstet Gynecol. 1997;  176 1328-1332 discussion 1332-1323
  • 138 Stevenson J T, Graham D J. Hepatic hemorrhage and the HELLP syndrome: a surgeon's perspective.  Am Surg. 1995;  61 756-760
  • 139 Erhard J, Lange R, Niebel W et al.. Acute liver necrosis in the HELLP syndrome: successful outcome after orthotopic liver transplantation. A case report.  Transpl Int. 1993;  6 179-181
  • 140 Hunter S K, Martin M, Benda J A, Zlatnik F J. Liver transplant after massive spontaneous hepatic rupture in pregnancy complicated by preeclampsia.  Obstet Gynecol. 1995;  85 819-822
  • 141 Strate T, Broering D C, Bloechle C et al.. Orthotopic liver transplantation for complicated HELLP syndrome. Case report and review of the literature.  Arch Gynecol Obstet. 2000;  264 108-111
  • 142 Greenstein D, Henderson J M, Boyer T D. Liver hemorrhage: recurrent episodes during pregnancy complicated by preeclampsia.  Gastroenterology. 1994;  106 1668-1671
  • 143 Ishak K G. Hepatic lesions caused by anabolic and contraceptive steroids.  Semin Liver Dis. 1981;  1 116-128

Yannick BacqM.D. 

Service d'Hépatogastroentérologie, Hôpital Trousseau

CHRU de Tours, 37044 Tours, France

Email: bacq@med.univ-tours.fr

    >