Background: Spontaneous hemoperitoneum in pregnancy (SHiP) is a rare, life-threatening event, particularly relevant to women with endometriosis or deciduosis. Methods: To determine the type of lesions leading to SHiP, a literature search was conducted among all published SHiP cases. From a total of 1,339 publications, information on pathological findings at the bleeding site with histological data was found in 24 case reports (16 pregnant, 8 postpartum). Results: Among pregnant women (81% primigravida), 75% had a diagnosis of endometriosis and 25% of deciduosis. Among postpartum women (38% primiparous), 63% had a diagnosis of deciduosis and 25% of endometriosis. In all cases except one, decidual cells, with or without glandular structures, were present at the bleeding site. Decidual vessels were described in 7 cases and all exhibited vascular changes, including distension of the lumen, medial disorganization, or loss of vascular integrity. These vessels were significantly different from arteries seen in the secretory endometrium, showing that structural modifications take place during the initial stage of the remodelling of placental bed spiral arteries. Conclusions: During pregnancy, a link seems to exist between ectopic decidualization, particularly that occurring in endometriotic foci, and occurrence of SHiP. In addition, subclinical decidual bleeding may be a potential risk factor for preterm labour.

Journal Section:
Editor's choice
Keywords:
Spontaneous hemoperitoneum, Endometriosis, Deciduosis, Pregnancy complications, In vitro fertilization
1.
Leone Roberti Maggiore U, Ferrero S, Mangili G, Bergamini A, Inversetti A, Giorgione V, Viganò P, Candiani M: A systematic review on endometriosis during pregnancy: diagnosis, misdiagnosis, complications and outcomes. Hum Reprod Update 2016;22:70-103.
2.
Brosens IA, Lier MC, Mijatovic V, Habiba M, Benagiano G: Severe spontaneous hemoperitoneum in pregnancy may be linked to in vitro fertilization in patients with endometriosis: a systematic review. Fertil Steril 2016;106:692-703.
3.
Hodgkinson CP, Christensen RC: Hemorrhage from ruptured utero-ovarian veins during pregnancy: report of 3 cases and review of the literature. Am J Obst Gynecol 1950;59:1112-1117.
4.
Ginsburg KA, Valdes C, Schnider G: Spontaneous utero-ovarian vessel rupture during pregnancy: three case reports and a review of the literature. Obstet Gynecol 1987;69(3 pt 2):474-476.
5.
Inoue T, Moriwaki T, Niki I: Endometriosis and spontaneous rupture of utero-ovarian vessels during pregnancy. Lancet 1992;340:240-241.
6.
Mizumoto Y, Furuya K, Kikuchi Y, Aida S, Hyakutake K, Tamai S, Nagata I: Spontaneous rupture of the uterine vessels in a pregnancy complicated by endometriosis. Acta Obstet Gynecol Scand 1996;75:860-862.
7.
Swaegers MC, Hauspy JJ, Buytaert PM, De Maeseneer MG: Spontaneous rupture of the uterine artery in pregnancy. Eur J Obstet Gynecol Reprod Biol 1997;75:145-146.
8.
Ismail KM, Shervington J: Hemoperitoneum secondary to pelvic endometriosis in pregnancy. Int J Gynaecol Obstet 1999;67:107-108.
9.
Janicki TI, David LJ, Skaf R: Massive and acute hemoperitoneum due to rupture of the uterine artery by erosion from an endometriotic lesion. Fertil Steril 2002;78:879-881.
10.
Hashimoto K, Tabata C, Ueno Y, Fukuda H, Shimoya K, Murata Y: Spontaneous rupture of uterine surface varicose veins in pregnancy: a case report. J Reprod Med 2006;51:722-724.
11.
Fiori O, Prugnolles H, Darai E, Uzan S, Berkane N: Spontaneous uterine artery rupture during pregnancy in a woman with sickle cell disease: a case report. J Reprod Med 2007;52:657-658.
12.
De Vincenzo R, Zannoni GF, Ricci C, Conte C, Masciullo V: Bowel endometriosis with hemoperitoneum complicating pregnancy. J Endometriosis 2011;5:166-169.
13.
Robboy SJ, Mutter GL, Prat J, Bentley RC, Russel P, Anderson MC: Robboy's Pathology of the Female Reproductive Tract, ed II. Amsterdam, Churchill Livingstone, Elsevier, 2008, p 579.
14.
Lier MCI, Malik RF, van Waesberghe JHTM, Maas JW, van Rumpt-van de Geest DA, Coppus SF, Berger JP, van Rijn BB, Janssen PF, de Boer MA, de Vries JIP, Jansen FW, Brosens IA, Lambalk CB, Mijatovic V: Spontaneous haemoperitoneum in pregnancy and endometriosis: a case series. BJOG 2017;124:306-312.
15.
Loh MJ, Wee JY, Teo SB: Endometriosis in a twin pregnancy leading to massive hemoperitoneum and intrauterine death: a case report. J Endometriosis 2015;7:86-88.
16.
Cozzolino M, Corioni S, Maggio L, Sorbi F, Guaschino S, Fambrini M: Endometriosis-related hemoperitoneum in pregnancy: a diagnosis to keep in mind. Ochsner J 2015;15:262-264.
17.
Aggarwal I, Tan P, Mathur M: Decidualised fallopian tube endometriotic implant causing spontaneous haemoperitoneum in a twin pregnancy. BMJ Case Rep 2014;pii:bcr2014205317.
18.
Kondoh E, Shimizu M, Kakui K, Mikami Y, Tatsumi K, Konishi I: Deciduosis can cause remarkable leukocytosis and obscure abdominal pain. J Obstet Gynaecol Res 2012;38:1376-1378.
19.
Reif P, Schöll W, Klaritsch P, Lang U: Rupture of endometriotic ovarian cyst causes acute hemoperitoneum in twin pregnancy. Fertil Steril 2011;95:2125.e1-e3.
20.
Brouckaert OM, Oostenveld E, Quartero H: Spontaneous hemoperitoneum and fetal demise in a nulliparous woman requiring hysterectomy with fetus in situ. Int J Gynaecol Obstet 2010;110:273.
21.
Bouet PE, Sentilhes L, Lefebvre-Lacoeuille C, Catala L, Gillard P, Descamps P: Endometriosis and spontaneous rupture of uterine vessels with hemothorax during pregnancy. Eur J Obstet Gynecol Reprod Biol 2009;144:95-96.
22.
Grunewald C, Jördens A: Intra-abdominal hemorrhage due to previously unknown endometriosis in the third trimester of pregnancy with uneventful neonatal outcome: a case report. Eur J Obstet Gynecol Reprod Biol 2010;148:204-205.
23.
Katorza E, Soriano D, Stockheim D, Mashiach R, Zolti M, Seidman DS, Schiff E, Goldenberg M: Severe intraabdominal bleeding caused by endometriotic lesions during the third trimester of pregnancy. Am J Obstet Gynecol 2007;197:501.e1-e4.
24.
Aziz U, Kulkarni A, Lazic D, Cullimore JE: Spontaneous rupture of the uterine vessels in pregnancy. Obstet Gynecol 2004;103:1089-1091.
25.
Doyle GB, Phillips DL: Fatal intraperitoneal haemorrhage during pregnancy. J Obstet Gynaecol Br Emp 1957;64:270-271.
26.
Zhang Z, Lou J: Hemoperitoneum after administration of prostaglandin E2 for induction of labour. Case Rep Obstet Gynecol 2015;2015:659274.
27.
Boztosun A, Sümer D, Çetin M, Ali Çetin A: Idiopathic spontaneous hemoperitoneum during early postpartum period: case report. Turkiye Klinikleri J Med Sci 2012;32:1718-1720.
28.
Gao JL, Lortie K, Singh SS: Laparoscopic internal iliac artery ligation for postpartum spontaneous hemoperitoneum. J Obstet Gynaecol Can 2010;32:1172-1175.
29.
O'Leary SM: Ectopic decidualization causing massive postpartum intraperitoneal hemorrhage. Obstet Gynecol 2006;108(3 pt 2):776-779.
30.
Richter MA, Choudhry A, Barton JJ, Merrick RE: Bleeding ectopic decidua as a cause of intraabdominal hemorrhage. A case report. J Reprod Med 1983;28:430-432.
31.
Sabatelle R, Winger E: Postpartum intraabdominal hemorrhage caused by ectopic deciduosis. Obstet Gynecol 1973;41:873-875.
32.
Hulme-Moir I, Ross MS: A case of early postpartum abdominal pain due to haemorrhagic deciduosis peritonei. J Obstet Gynaecol Br Commonw 1969;76:746-749.
33.
Craven CM, Morgan T, Ward K: Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta 1998;19:241-252.
34.
Brosens I, Pijnenborg R, Vercruysse L, Romero R: The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 2011;204:193-201.
35.
Zaytsev P, Taxy JB: Pregnancy-associated ectopic decidua. Am J Surg Pathol 1987;11:526-530.
36.
Büttner A, Bässler R, Theele C: Pregnancy-associated ectopic decidua (deciduosis) of the greater omentum. An analysis of 60 biopsies with cases of fibrosing deciduosis and leiomyomatosis peritonealis disseminata. Pathol Res Pract 1993;189:352-359.
37.
Markou GA, Goubin-Versini I, Carbunaru OM, Karatzios C, Muray JM, Fysekidis M: Macroscopic deciduosis in pregnancy is finally a common entity. Eur J Obstet Gynecol Reprod Biol 2016;197:54-58.
38.
Bulun SE, Cheng YH, Yin P, Imir G, Utsunomiya H, Attar E, Innes J, Julie Kim J: Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol Cell Endocrinol 2006;248:94-103.
39.
Brosens IA, Fusi L, Brosens JJ: Endometriosis is a risk factor for spontaneous hemoperitoneum during pregnancy. Fertil Steril 2009;92:1243-1245.
40.
Smith SD, Choudhury RH, Matos P, Horn JA, Lye SJ, Dunk CE, Aplin JD, Jones RL, Harris LK: Changes in vascular extracellular matrix composition during decidual spiral arteriole remodeling in early human pregnancy. Histol Histopathol 2016;31:557-571.
41.
Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O: Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006;12:1065-1074.
42.
Dunn CL, Kelly RW, Critchley HO: Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod BioMed Online 2003;7:151-161.
43.
Lash GE, Otun HA, Innes BA, Kirkley M, De Oliveira L, Searle RF, Robson SC, Bulmer JN: Interferon-gamma inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels. FASEB J 2006;20:2512-2518.
44.
Lockwood CJ, Kayisli UA, Stocco C, Murk W, Vatandaslar E, Buchwalder LF, Schatz F: Abruption-induced preterm delivery is associated with thrombin-mediated functional progesterone withdrawal in decidual cells. Am J Pathol 2012;181:2138-2148.
45.
Kim YM, Bujold E, Chaiworapongsa T, Gomez R, Yoon BH, Thaler HT, Rotmensch S, Romero R: Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2003;189:1063-1069.
46.
Romero R, Dey SK, Fisher SJ: Preterm labor: one syndrome, many causes. Science 2014;345:760-765.
47.
Chaiworapongsa T, Romero R, Whitten AE, Korzeniewski SJ, Chaemsaithong P, Hernandez-Andrade E, Yeo L, Hassan SS: 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 Fetal Neonatal Med 2016;29:1214-1228.
48.
Marcellin L, Santulli P, Gogusev J, Lesaffre C, Jacques S, Chapron C, Goffinet F, Vaiman D, Mehats C: Endometriosis also affects the decidua in contact with the fetal membranes during pregnancy. Hum Reprod 2015:30:392-405.
49.
Salafia CM, Pezzullo JC, López-Zeno JA, Simmens S, Minior VK, Vintzileos AM: Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 1995;173:1097-1105.
50.
Sakata M, Sado T, Kitanaka T, Naruse K, et al: Iron-dependent oxidative stress as a pathogenesis for preterm birth. Obstet Gynecol Surv 2008;63:651-660.
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