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Endometriosis is a risk factor for spontaneous hemoperitoneum during pregnancy

2009; Elsevier BV; Volume: 92; Issue: 4 Linguagem: Inglês

10.1016/j.fertnstert.2009.03.091

1556-5653

Ivo Brosens, Luca Fusi, Jan J. Brosens,

Uterine Myomas and Treatments

Spontaneous hemoperitoneum in pregnancy (SHiP) is a rare but dramatic cause of perinatal mortality and morbidity. Emerging evidence suggests that pelvic endometriosis may play an important role in the pathogenesis of SHiP. Spontaneous hemoperitoneum in pregnancy (SHiP) is a rare but dramatic cause of perinatal mortality and morbidity. Emerging evidence suggests that pelvic endometriosis may play an important role in the pathogenesis of SHiP. Spontaneous hemoperitoneum in pregnancy (SHiP) has been recognized for more than a century as a relatively rare disorder associated with a high perinatal mortality rate. Unprovoked peritoneal bleeding has been reported to occur during the second half of pregnancy, in labor, and occasionally during the early postpartum period. The major symptoms are acute or subacute abdominal pain, followed by hypovolemic shock and fetal distress. In 1950, a review of 75 cases reported an overall maternal mortality rate of 49.3% (1Hodgkinson C.P. Christensen R.C. Hemorrhage from ruptured utero-ovarian veins during pregnancy; report of 3 cases and review of the literature.Am J Obstet Gynecol. 1950; 59: 1112-1117Abstract Full Text PDF PubMed Scopus (92) Google Scholar). Although maternal mortality associated with SHiP dropped dramatically between 1950 and 1987, fetal mortality remained high, at 31% (2Ginsburg K.A. Valdes C. Schnider G. Spontaneous utero-ovarian vessel rupture during pregnancy: three case reports and a review of the literature.Obstet Gynecol. 1987; 69: 474-476PubMed Google Scholar). The present study reviews all cases of SHiP published during the last 20 years with the aim of assessing its associated risk factors and formulating recommendations for improving pregnancy outcome. A search of Pubmed and Scopus, from January 1987 to August 2008, was carried out, not restricted by language, for publications in peer-reviewed journals with the following key words: "hemoperitoneum," "spontaneous vessel rupture," "pregnancy," and "endometriosis." Twenty publications, reporting a total of 25 cases, were retrieved (3Aziz U. Kulkarni A. Lazic D. Cullimore J.E. Spontaneous rupture of the uterine vessels in pregnancy.Obstet Gynecol. 2004; 103: 1089-1091Crossref PubMed Google Scholar, 4Bellucci M.J. Burke M.C. Querusio L. Atraumatic rupture of utero-ovarian vessels during pregnancy: a lethal presentation of maternal shock.Ann Emerg Med. 1994; 23: 360-362Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar, 5Chiodo I. Somigliana E. Dousset B. Chapron C. Urohemoperitoneum during pregnancy with consequent fetal death in a patient with deep endometriosis.J Minim Invasive Gynecol. 2008; 15: 202-204Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 6Dubuisson J. Pennehouat G. Rudigoz R.C. [Spontaneous rupture of the uterine pedicle during pregnancy: three case reports].Gynecol Obstet Fertil. 2006; 34: 711-715Crossref PubMed Scopus (10) Google Scholar, 7Fiori 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: 657-658PubMed Google Scholar, 8Hashimoto 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: 722-724PubMed Google Scholar, 9Inoue T. Moriwaki T. Niki I. Endometriosis and spontaneous rupture of utero-ovarian vessels during pregnancy.Lancet. 1992; 340: 240-241Abstract PubMed Scopus (40) Google Scholar, 10Ismail K.M. Shervington J. Hemoperitoneum secondary to pelvic endometriosis in pregnancy.Int J Gynaecol Obstet. 1999; 67: 107-108Crossref PubMed Scopus (17) Google Scholar, 11Kalaichandran S. Spontaneous haemoperitoneum in labour from ruptured utero-ovarian vessels.J R Soc Med. 1991; 84: 372-373Crossref PubMed Scopus (8) Google Scholar, 12Katorza E. Soriano D. Stockheim D. Mashiach R. Zolti M. Seidman D.S. et al.Severe intraabdominal bleeding caused by endometriotic lesions during the third trimester of pregnancy.Am J Obstet Gynecol. 2007; 197 (501.e1–4)Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 13Koifman A. Weintraub A.Y. Segal D. Idiopathic spontaneous hemoperitoneum during pregnancy.Arch Gynecol Obstet. 2007; 276: 269-270Crossref PubMed Scopus (17) Google Scholar, 14Leung W.C. Leung T.W. Lam Y.H. Haemoperitoneum due to cornual endometriosis during pregnancy resulting in intrauterine death.Aust N Z J Obstet Gynaecol. 1998; 38: 156-157Crossref PubMed Scopus (11) Google Scholar, 15Mizumoto Y. Furuya K. Kikuchi Y. Aida S. Hyakutake K. Tamai S. et al.Spontaneous rupture of the uterine vessels in a pregnancy complicated by endometriosis.Acta Obstet Gynecol Scand. 1996; 75: 860-862Crossref PubMed Scopus (33) Google Scholar, 16Passos F. Calhaz-Jorge C. Graca L.M. Endometriosis is a possible risk factor for spontaneous hemoperitoneum in the third trimester of pregnancy.Fertil Steril. 2008; 89: 251-252Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 17Renuka T. Dhaliwal L.K. Gupta I. Hemorrhage from ruptured utero-ovarian veins during pregnancy.Int J Gynaecol Obstet. 1998; 60: 167-168Crossref PubMed Scopus (19) Google Scholar, 18Roger N. Chitrit Y. Souhaid A. Rezig K. Saint-Leger S. [Intraperitoneal hemorrhage from rupture of uterine varicose vein during pregnancy: case report and review of the literature].J Gynecol Obstet Biol Reprod (Paris). 2005; 34 (French): 497-500Crossref PubMed Google Scholar, 19Rosales R.G. Saldana M.A.C. Leal I.A. Lopez J.A.C. Rotura espontanea de los vasos uterinos durante el embarazo: communicacion de un caso y revision bibliografia.Ginecologia y Obstetricia de Mexico. 2008; 76: 221-223PubMed Google Scholar, 20Swaegers M.C. Hauspy J.J. Buytaert P.M. De Maeseneer M.G. Spontaneous rupture of the uterine artery in pregnancy.Eur J Obstet Gynecol Reprod Biol. 1997; 75: 145-146Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar, 21Vellekoop J. de Leeuw J.P. Neijenhuis P.A. Spontaneous rupture of a utero-ovarian vein during pregnancy.Am J Obstet Gynecol. 2001; 184: 241-242Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 22Wu C.-Y. Hwang J.-L. Lin Y.-H. Hsieh B.-C. Seow K.-M. Huang L.-W. Spontaneous hemopertineum in pregnancy from a ruptured superficial uterine vessel.Taiwan J Obstet Gynecol. 2007; 46: 77-80Crossref PubMed Scopus (16) Google Scholar). Data were analyzed using Pearson chi-squared (χ2) test or two-tailed unpaired t test, with the level of significance defined as P<.05. For this review paper, Institutional Review Board approval was not sought. Nulliparous women represented 72% of cases of SHiP (18 out of 25; Table 1). The mean age was 30 (SD ±4.4) years. The main presenting symptom was sudden onset of acute or subacute abdominal pain during the second half of pregnancy. In all cases, abdominal ultrasound examination revealed no signs of placental abruption and failed to diagnose intraperitoneal bleeding as a cause of acute pain. Transvaginal ultrasound and computerized tomography scans sometimes indicated the presence of intraperitoneal free fluid, but in most cases the diagnosis was only established at laparotomy, which was carried out for maternal reasons (hypovolemic shock and progressive anemia; n = 14), for fetal reasons (fetal distress; n = 10), or both (n = 1).Table 1Spontaneous hemoperitoneum in pregnancy (SHiP): demographic data and clinical outcome.ReferenceAgeParityGestation (weeks)Endometriosis (rAFS stage)OutcomeRosales et al. 19Rosales R.G. Saldana M.A.C. Leal I.A. Lopez J.A.C. Rotura espontanea de los vasos uterinos durante el embarazo: communicacion de un caso y revision bibliografia.Ginecologia y Obstetricia de Mexico. 2008; 76: 221-223PubMed Google Scholar23?22—NL (38 w)Fiori 7Fiori 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: 657-658PubMed Google Scholar28037—NLWu et al. 22Wu C.-Y. Hwang J.-L. Lin Y.-H. Hsieh B.-C. Seow K.-M. Huang L.-W. Spontaneous hemopertineum in pregnancy from a ruptured superficial uterine vessel.Taiwan J Obstet Gynecol. 2007; 46: 77-80Crossref PubMed Scopus (16) Google ScholaraSHiP after IVF-ET.31133 (twins)Yes (III)NL/NLChiodo et al. 5Chiodo I. Somigliana E. Dousset B. Chapron C. Urohemoperitoneum during pregnancy with consequent fetal death in a patient with deep endometriosis.J Minim Invasive Gynecol. 2008; 15: 202-204Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar22031Yes (IV)SBKoifman et al. 13Koifman A. Weintraub A.Y. Segal D. Idiopathic spontaneous hemoperitoneum during pregnancy.Arch Gynecol Obstet. 2007; 276: 269-270Crossref PubMed Scopus (17) Google Scholar24037—NLHashimoto et al. 8Hashimoto 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: 722-724PubMed Google Scholar40233—NLDubuisson et al. 6Dubuisson J. Pennehouat G. Rudigoz R.C. [Spontaneous rupture of the uterine pedicle during pregnancy: three case reports].Gynecol Obstet Fertil. 2006; 34: 711-715Crossref PubMed Scopus (10) Google Scholar25030—NND36032PFSB31030—SBPassos et al. 16Passos F. Calhaz-Jorge C. Graca L.M. Endometriosis is a possible risk factor for spontaneous hemoperitoneum in the third trimester of pregnancy.Fertil Steril. 2008; 89: 251-252Abstract Full Text Full Text PDF PubMed Scopus (33) Google ScholaraSHiP after IVF-ET.30032 (twins)Yes (III)NL/NL32031Yes (III)NLKatorza et al. 12Katorza E. Soriano D. Stockheim D. Mashiach R. Zolti M. Seidman D.S. et al.Severe intraabdominal bleeding caused by endometriotic lesions during the third trimester of pregnancy.Am J Obstet Gynecol. 2007; 197 (501.e1–4)Abstract Full Text Full Text PDF PubMed Scopus (33) Google ScholaraSHiP after IVF-ET.29028 (twins)Yes (I)RDS/RDS31126Yes (III)SB32029Yes (III)CPRoger et al. 18Roger N. Chitrit Y. Souhaid A. Rezig K. Saint-Leger S. [Intraperitoneal hemorrhage from rupture of uterine varicose vein during pregnancy: case report and review of the literature].J Gynecol Obstet Biol Reprod (Paris). 2005; 34 (French): 497-500Crossref PubMed Google Scholar34127PFNL (38 w)Aziz et al. 3Aziz U. Kulkarni A. Lazic D. Cullimore J.E. Spontaneous rupture of the uterine vessels in pregnancy.Obstet Gynecol. 2004; 103: 1089-1091Crossref PubMed Google Scholar30020Yes (I)SBVellekoop 21Vellekoop J. de Leeuw J.P. Neijenhuis P.A. Spontaneous rupture of a utero-ovarian vein during pregnancy.Am J Obstet Gynecol. 2001; 184: 241-242Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar31025—NL (38 w)Ismail and Shervington 10Ismail K.M. Shervington J. Hemoperitoneum secondary to pelvic endometriosis in pregnancy.Int J Gynaecol Obstet. 1999; 67: 107-108Crossref PubMed Scopus (17) Google Scholar?033Yes (I)NLRenuka et al. 17Renuka T. Dhaliwal L.K. Gupta I. Hemorrhage from ruptured utero-ovarian veins during pregnancy.Int J Gynaecol Obstet. 1998; 60: 167-168Crossref PubMed Scopus (19) Google Scholar25136—SBLeung et al. 14Leung W.C. Leung T.W. Lam Y.H. Haemoperitoneum due to cornual endometriosis during pregnancy resulting in intrauterine death.Aust N Z J Obstet Gynaecol. 1998; 38: 156-157Crossref PubMed Scopus (11) Google Scholar35033Yes (I)SBSwaegers et al. 20Swaegers M.C. Hauspy J.J. Buytaert P.M. De Maeseneer M.G. Spontaneous rupture of the uterine artery in pregnancy.Eur J Obstet Gynecol Reprod Biol. 1997; 75: 145-146Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar29033—NLMizumoto et al. 15Mizumoto Y. Furuya K. Kikuchi Y. Aida S. Hyakutake K. Tamai S. et al.Spontaneous rupture of the uterine vessels in a pregnancy complicated by endometriosis.Acta Obstet Gynecol Scand. 1996; 75: 860-862Crossref PubMed Scopus (33) Google Scholar28028Yes (II)NNDBellucci et al. 4Bellucci M.J. Burke M.C. Querusio L. Atraumatic rupture of utero-ovarian vessels during pregnancy: a lethal presentation of maternal shock.Ann Emerg Med. 1994; 23: 360-362Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar30134—NLKalaichandran 11Kalaichandran S. Spontaneous haemoperitoneum in labour from ruptured utero-ovarian vessels.J R Soc Med. 1991; 84: 372-373Crossref PubMed Scopus (8) Google Scholar33029—NNDInoue et al. 9Inoue T. Moriwaki T. Niki I. Endometriosis and spontaneous rupture of utero-ovarian vessels during pregnancy.Lancet. 1992; 340: 240-241Abstract PubMed Scopus (40) Google Scholar37029Yes (III)NLNote: CP = cerebral palsy; NL = normal; NND = neonatal death; PF = parametrial fenestration or laceration (Allan-Masters syndrome); RDS = respiratory distress syndrome; SB = stillborn.a SHiP after IVF-ET. Open table in a new tab Note: CP = cerebral palsy; NL = normal; NND = neonatal death; PF = parametrial fenestration or laceration (Allan-Masters syndrome); RDS = respiratory distress syndrome; SB = stillborn. At laparotomy, a substantial amount of intra-abdominal blood was found, estimated to vary between 500 and 4,000 mL. Active bleeding was observed in all but three cases (Table 1). In one of them, a parametrial laceration was coagulated at 27 weeks' gestation, which allowed the pregnancy to continue (18Roger N. Chitrit Y. Souhaid A. Rezig K. Saint-Leger S. [Intraperitoneal hemorrhage from rupture of uterine varicose vein during pregnancy: case report and review of the literature].J Gynecol Obstet Biol Reprod (Paris). 2005; 34 (French): 497-500Crossref PubMed Google Scholar), whereas in the other two cases cesarean sections were performed at 34 and 37 weeks (13Koifman A. Weintraub A.Y. Segal D. Idiopathic spontaneous hemoperitoneum during pregnancy.Arch Gynecol Obstet. 2007; 276: 269-270Crossref PubMed Scopus (17) Google Scholar, 16Passos F. Calhaz-Jorge C. Graca L.M. Endometriosis is a possible risk factor for spontaneous hemoperitoneum in the third trimester of pregnancy.Fertil Steril. 2008; 89: 251-252Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar). In two cases with active bleeding, at 22 and 25 weeks hemostatic sutures or clips were applied and both pregnancies continued normally to term (19Rosales R.G. Saldana M.A.C. Leal I.A. Lopez J.A.C. Rotura espontanea de los vasos uterinos durante el embarazo: communicacion de un caso y revision bibliografia.Ginecologia y Obstetricia de Mexico. 2008; 76: 221-223PubMed Google Scholar, 21Vellekoop J. de Leeuw J.P. Neijenhuis P.A. Spontaneous rupture of a utero-ovarian vein during pregnancy.Am J Obstet Gynecol. 2001; 184: 241-242Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar). One patient underwent hysterectomy after cesarean section, because of multiple bleeding sites from varicose veins on the posterior uterine surface (8Hashimoto 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: 722-724PubMed Google Scholar). No maternal deaths were reported. There were three twin pregnancies among the 25 reported cases of SHiP, all conceived after IVF treatment. There were ten cases of fetal or neonatal death, resulting in a perinatal mortality rate of 36% (10 out of 28; Table 1), which compares unfavorably to the 31% reported by Ginsburg et al. in 1987 (2Ginsburg K.A. Valdes C. Schnider G. Spontaneous utero-ovarian vessel rupture during pregnancy: three case reports and a review of the literature.Obstet Gynecol. 1987; 69: 474-476PubMed Google Scholar). Recurrence of SHiP has not been reported in subsequent pregnancies (6Dubuisson J. Pennehouat G. Rudigoz R.C. [Spontaneous rupture of the uterine pedicle during pregnancy: three case reports].Gynecol Obstet Fertil. 2006; 34: 711-715Crossref PubMed Scopus (10) Google Scholar, 11Kalaichandran S. Spontaneous haemoperitoneum in labour from ruptured utero-ovarian vessels.J R Soc Med. 1991; 84: 372-373Crossref PubMed Scopus (8) Google Scholar). The bleeding was described as venous, arterial, or unknown in 20 (80%), 4 (16%), and 1 (4%) case, respectively. Strikingly, the bleeding site in 90% of cases was either the posterior side of the uterus or the parametrium. As shown in Table 1, endometriosis is a major risk factor for SHiP. Of the 13 cases (52%), six women were known to have endometriosis diagnosed by laparoscopy prior to pregnancy, six were diagnosed at the time of laparotomy, and in one case the diagnosis was made 3 months after delivery at the time of laparoscopy for persistent pelvic pain (12Katorza E. Soriano D. Stockheim D. Mashiach R. Zolti M. Seidman D.S. et al.Severe intraabdominal bleeding caused by endometriotic lesions during the third trimester of pregnancy.Am J Obstet Gynecol. 2007; 197 (501.e1–4)Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar). As shown in Table 1, the stage of endometriosis varied from minimal and mild (n = 6) to severe (n = 7). Biopsy samples of the site of bleeding during pregnancy were obtained in five cases and, strikingly, all specimens contained endometriosis, characterized by prominent vascularization and decidualization of the lesion (3Aziz U. Kulkarni A. Lazic D. Cullimore J.E. Spontaneous rupture of the uterine vessels in pregnancy.Obstet Gynecol. 2004; 103: 1089-1091Crossref PubMed Google Scholar, 5Chiodo I. Somigliana E. Dousset B. Chapron C. Urohemoperitoneum during pregnancy with consequent fetal death in a patient with deep endometriosis.J Minim Invasive Gynecol. 2008; 15: 202-204Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 10Ismail K.M. Shervington J. Hemoperitoneum secondary to pelvic endometriosis in pregnancy.Int J Gynaecol Obstet. 1999; 67: 107-108Crossref PubMed Scopus (17) Google Scholar, 12Katorza E. Soriano D. Stockheim D. Mashiach R. Zolti M. Seidman D.S. et al.Severe intraabdominal bleeding caused by endometriotic lesions during the third trimester of pregnancy.Am J Obstet Gynecol. 2007; 197 (501.e1–4)Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 15Mizumoto Y. Furuya K. Kikuchi Y. Aida S. Hyakutake K. Tamai S. et al.Spontaneous rupture of the uterine vessels in a pregnancy complicated by endometriosis.Acta Obstet Gynecol Scand. 1996; 75: 860-862Crossref PubMed Scopus (33) Google Scholar). Patients with and without endometriosis did not differ in age, parity, or gestation, but notably all cases of SHiP after IVF treatment (n = 6) occurred in women with endometriosis. Perinatal mortality rates were also similar between patients with and without documented endometriosis. However, the likelihood of adverse pregnancy outcome, which takes in account the perinatal mortality rate as well as the three infants with severe perinatal morbidity, was significantly higher in the endometriosis group (P=.01). A recurrent theme in this review is that SHiP is not diagnosed until explorative laparotomy becomes inevitable. In all but four cases, the bleeding was not arterial but arose from superficial veins or varicosities on the posterior surface of the uterus or parametria, suggesting that prompt diagnosis and timely intervention can prevent adverse pregnancy outcome. This is further illustrated by three cases where coagulation or ligature of the bleeding vessels or laceration allowed the pregnancy to continue normally (18Roger N. Chitrit Y. Souhaid A. Rezig K. Saint-Leger S. [Intraperitoneal hemorrhage from rupture of uterine varicose vein during pregnancy: case report and review of the literature].J Gynecol Obstet Biol Reprod (Paris). 2005; 34 (French): 497-500Crossref PubMed Google Scholar, 19Rosales R.G. Saldana M.A.C. Leal I.A. Lopez J.A.C. Rotura espontanea de los vasos uterinos durante el embarazo: communicacion de un caso y revision bibliografia.Ginecologia y Obstetricia de Mexico. 2008; 76: 221-223PubMed Google Scholar, 21Vellekoop J. de Leeuw J.P. Neijenhuis P.A. Spontaneous rupture of a utero-ovarian vein during pregnancy.Am J Obstet Gynecol. 2001; 184: 241-242Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar). Awareness of the risk factors associated with SHiP may facilitate the diagnosis and expedite intervention. One such risk factor, especially in IVF patients, is endometriosis, as previously alluded to by others (9Inoue T. Moriwaki T. Niki I. Endometriosis and spontaneous rupture of utero-ovarian vessels during pregnancy.Lancet. 1992; 340: 240-241Abstract PubMed Scopus (40) Google Scholar, 12Katorza E. Soriano D. Stockheim D. Mashiach R. Zolti M. Seidman D.S. et al.Severe intraabdominal bleeding caused by endometriotic lesions during the third trimester of pregnancy.Am J Obstet Gynecol. 2007; 197 (501.e1–4)Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 15Mizumoto Y. Furuya K. Kikuchi Y. Aida S. Hyakutake K. Tamai S. et al.Spontaneous rupture of the uterine vessels in a pregnancy complicated by endometriosis.Acta Obstet Gynecol Scand. 1996; 75: 860-862Crossref PubMed Scopus (33) Google Scholar, 23Noack E.J. Hohlweg-Majert P. [Spontaneous rupture of a deciduoma with intra-abdominal hemorrhage].Geburtshilfe Frauenheilkd. 1984; 44: 263-264Crossref PubMed Scopus (3) Google Scholar). Peritoneal endometriotic implants undergo decidual changes in the first trimester of pregnancy, characterized by loss of pigmentation and fibrosis, which renders visual diagnosis more difficult (24Moen M.H. Muus K.M. Endometriosis in pregnant and nonpregnant women at tubal sterilization.Hum Reprod. 1991; 6: 699-702Crossref PubMed Scopus (95) Google Scholar). Therefore, it appears likely that if no biopsy is taken, decidualized endometriosis is often missed at the time of an emergency laparotomy for SHiP. Invasiveness of severe endometriosis has been suggested as a reason for SHiP, but we found no apparent correlation between SHiP and stage of endometriosis. An alternative explanation is that SHiP results from involution of decidualizing ectopic endometrium during pregnancy. Decidualization represents in the differentiation of mesenchymal cells "the point of no return," after which the cellular integrity becomes inextricably dependent upon sustained progesterone signaling (25Brosens J.J. Gellersen B. Death or survival—progesterone-dependent cell fate decisions in the human endometrial stroma.J Mol Endocrinol. 2006; 36: 389-398Crossref PubMed Scopus (105) Google Scholar). Falling progesterone levels not only reverse the decidual phenotype, but also induce the expression of a gene network that encodes for chemokines, proinflammatory cytokines, matrix metalloproteinases, and apoptotic factors, leading to influx of inflammatory cells, proteolytic breakdown of the extracellular matrix, cell death, and bleeding. Interestingly, emerging evidence suggests that endometriosis is associated with progesterone resistance, characterized by suboptimal expression of target genes (26Burney R.O. Talbi S. Hamilton A.E. Vo K.C. Nyegaard M. Nezhat C.R. et al.Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis.Endocrinology. 2007; 148: 3814-3826Crossref PubMed Scopus (552) Google Scholar). Therefore, it is tempting to speculate that "functional" progesterone withdrawal triggers involution of the decidual phenotype of the ectopic endometrium surrounding distended parametrial veins, leading to peritoneal bleeding of unpredictable severity. Massive spontaneous hemoperitoneum associated with mild endometriosis has also been described in the postpartum period and at the time of menstruation (27Fiadjoe P. Thomas-Phillips A. Reddy K. Massive haemoperitoneum due to uterine artery erosion by endometriosis and a review of the literature.Gynecol Surg. 2008; 5: 133-135Crossref Scopus (5) Google Scholar, 28O'Leary S.M. Ectopic decidualization causing massive postpartum intraperitoneal hemorrhage.Obstet Gynecol. 2006; 108: 776-779Crossref PubMed Scopus (49) Google Scholar, 29Uri F.I. Opaneye A. Haemoperitoneum due to cornual endometriosis after laparoscopic sterilisation.Br J Obstet Gynaecol. 1979; 86: 664-665Crossref PubMed Scopus (5) Google Scholar). In addition, rupture of sigmoid or appendix during late pregnancy in nulliparous women has been related to decidualization of endometriotic implants (30Clement P.B. Perforation of the sigmoid colon during pregnancy: a rare complication of endometriosis.Case report. Br J Obstet Gynaecol. 1977; 84: 548-550Crossref PubMed Scopus (38) Google Scholar, 31Gini P.C. Chukudebelu W.O. Onuigbo W.I. Perforation of the appendix during pregnancy: a rare complication of endometriosis.Case report. Br J Obstet Gynaecol. 1981; 88: 456-458Crossref PubMed Scopus (48) Google Scholar, 32Loverro G. Cormio G. Greco P. Altomare D. Putignano G. Selvaggi L. Perforation of the sigmoid colon during pregnancy: a rare complication of endometriosis.J Gynecol Surg. 1999; 15: 155-157Crossref Scopus (10) Google Scholar). Whereas pregnancy may have a beneficial effect on endometriosis by promoting involution of implants and, as recently suggested, endometriosis may confer protection against preeclampsia (33Brosens JJ, Parker MG, McIndoe A, PijnenborgI R, Brosens IA. A role for menstruation in preconditioning the uterus for successful pregnancy. Am J Obstet Gynecol Published online January 10, 2009 [Epub ahead of print].Google Scholar), rare but important endometriosis-associated pregnancy complications also exist. In summary, a greater awareness of SHiP and its associated risk factors, such as pelvic endometriosis, is needed to improve perinatal outcome in years to come.