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Management of postabortion hemorrhage

      Abstract

      Hemorrhage after abortion is rare, occurring in fewer than 1% of abortions, but associated morbidity may be significant. Hemorrhage can be caused by atony, coagulopathy and abnormal placentation, as well as by such procedure complications as perforation, cervical laceration and retained tissue. Evidence on which to make recommendations regarding risk factors and treatment for postabortion hemorrhage is extremely limited. Although medical abortion is associated with more bleeding than surgical abortion, overall bleeding for the two methods is minimal and not clinically different. Identifying patients who may be at increased risk of hemorrhage can help reduce blood loss with abortion. Specifically, women with a uterine scar and complete placenta previa seeking abortion at gestations greater than 16 weeks should be evaluated for placenta accreta. For women at high risk of hemorrhage, referral to a high-acuity center should be considered. We propose an algorithm for treating postabortion hemorrhage as follows: (1) assessment and exam, (2) massage and medical therapy, (3) resuscitative measures with laboratory evaluation and possible re-aspiration or balloon tamponade, and (4) interventions such as embolization and surgery. The Society of Family Planning recommends preoperative identification of women at high risk of hemorrhage as well as development of an organized approach to treatment. Further studies are needed on prophylactic use of uterotonic medication, intraoperative ultrasound and optimal delivery of the placenta after second-trimester medical abortion.

      Keywords

      Since abortion was legalized in 1973, abortion-related mortality and morbidity have declined sharply [
      • Bartlett L.A.
      • Berg C.J.
      • Shulman H.B.
      • et al.
      Risk factors for legal induced abortion-related mortality in the United States.
      ]. Abortion in the United States is a very safe procedure, with minor complications occurring in an estimated 8 per 1,000 abortions, major complications occurring in 0.7 per 1,000 abortions, and mortality occurring in 0.7 per 100,000 legal abortions per year [
      • Hakim-Elahi E.
      • Tovell H.M.
      • Burnhill M.S.
      Complications of first-trimester abortion: a report of 170,000 cases.
      ]. The most common causes of mortality have changed over time. In the decade after legalization, anesthetic complications accounted for the highest percentage of deaths. Today, hemorrhage is the most common cause of abortion-related mortality in the second trimester, accounting for 33% and 40% of deaths following second-trimester induction termination and dilation and evacuation (D&E) [

      Paul M, Lichtenberg ES, Borgatta L, Grimes DA, Stubblefield PG, Creinin MD. Management of Unintended and Abnormal Pregnancy: Comprehensive Abortion Care. Chichester, West Sussex, UK: John Wiley & Sons, Ltd, 2009. p. 376. [Evidence Grade: III]

      ]. In the first trimester, infection is the most common cause of abortion-related mortality (33%), with hemorrhage accounting for 14% of deaths.
      Hemorrhage after abortion has been variably defined across studies, making comparisons of incidence, risk factors and treatment difficult. Definitions of postabortion hemorrhage include “greater than 250 mL blood loss,” “greater than 500 mL blood loss,” “requiring hospitalization” and “requiring transfusion.” A clinically relevant definition would include both a clinical response to excessive bleeding, such as transfusion or admission, and/or bleeding in excess of 500 mL.
      Estimates of hemorrhage after vacuum aspiration in the first trimester range from 0 to 3 per 1,000 cases [
      • Hakim-Elahi E.
      • Tovell H.M.
      • Burnhill M.S.
      Complications of first-trimester abortion: a report of 170,000 cases.
      ,

      National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

      ,
      • Chen L.
      • Lai S.
      • Lee W.
      • Leong N.
      Uterine perforation during elective first trimester abortions: a 13-year review.
      ,
      • Choudhary N.
      • Saha S.C.
      • Gopalan S.
      Abortion procedures in a tertiary care institution in India.
      ]. Although hemorrhage immediately after first-trimester abortion is rare, delayed bleeding is more common. Two recent, large, registry-based cohort studies found that 1–2% of patients who underwent first-trimester surgical abortion had bleeding that necessitated a visit or secondary surgical intervention [
      • Engbaek J.
      • Bartholdy J.
      • Hjortso N.C.
      Return hospital visits and morbidity within 60 days after day surgery: a retrospective study of 18,736 day surgical procedures.
      ,
      • Niinimaki M.
      • Pouta A.
      • Bloigu A.
      • et al.
      Immediate complications after medical compared with surgical termination of pregnancy.
      ]. These studies lacked a consistent definition of bleeding, and likely represent overestimates of excessive bleeding after first-trimester abortion. Hemorrhage after surgical abortion is more common in the second trimester than the first, with estimates ranging from 0.9 to 10 per 1,000 cases [
      • Altman A.M.
      • Stubblefield P.G.
      • Schlam J.F.
      • Loberfeld R.
      • Osathanondh R.
      Midtrimester abortion with laminaria and vacuum evacuation on a teaching service.
      ,
      • Castleman L.D.
      • Oanh K.T.
      • Hyman A.G.
      • Thuy le T.
      • Blumenthal P.D.
      Introduction of the dilation and evacuation procedure for second-trimester abortion in Vietnam using manual vacuum aspiration and buccal misoprostol.
      ,
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ,
      • Patel A.
      • Talmont E.
      • Morfesis J.
      • et al.
      Adequacy and safety of buccal misoprostol for cervical preparation prior to termination of second-trimester pregnancy.
      ,
      • Peterson W.F.
      • Berry F.N.
      • Grace M.R.
      • Gulbranson C.L.
      Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
      ].

      Etiologies

      Known etiologies include perforation, cervical laceration, retained tissue, abnormal placentation, atony and coagulopathy (Table 1). Little is known about population-relative frequencies of each of these causes because of the low incidence of hemorrhage, inconsistent definitions of hemorrhage and a paucity of studies. In a case series from 2008 by Steinauer et al. of 42 women requiring uterine artery embolization (UAE) for severe hemorrhage, the causes of hemorrhage in order of frequency were atony (52%), abnormal placentation (17%), cervical laceration (12%), perforation (7%), lower uterine segment bleeding without atony (5%) and disseminated intravascular coagulopathy (5%) [
      • Steinauer J.E.
      • Diedrich J.T.
      • Wilson M.W.
      • Darney P.D.
      • Vargas J.E.
      • Drey E.A.
      Uterine artery embolization in postabortion hemorrhage.
      ].
      Table 1Causes of postabortion hemorrhage and associated risk factors
      Cause of hemorrhageRisk factors
      AtonyPrior cesarean section 
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      Use of halogenated anesthetic agents
      • Kumarasinghe N.
      • Harpin R.
      • Stewart A.W.
      Blood loss during suction termination of pregnancy with two different anaesthetic techniques.
      Gestational age ≥20 weeks
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      Increasing maternal age
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      Cervical lacerationSurgical inexperience
      • Grimes D.
      • Schulz K.
      • Cates Jr., W.
      Prevention of uterine perforation during curettage abortion.
      ,
      • Schulz K.
      • Grimes D.
      • Cates Jr., W.
      Measures to prevent cervical injury during suction curettage abortion.
      Inadequate cervical dilation
      • Peterson W.F.
      • Berry F.N.
      • Grace M.R.
      • Gulbranson C.L.
      Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
      Nulliparity
      • Newmann S.
      • Dalve-Endres A.
      • Drey E.A.
      Clinical guidelines. Cervical preparation for surgical abortion from 20 to 24 weeks' gestation.
      Gestational age ≥20 weeks
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ,
      • Newmann S.
      • Dalve-Endres A.
      • Drey E.A.
      Clinical guidelines. Cervical preparation for surgical abortion from 20 to 24 weeks' gestation.
      PerforationSurgical inexperience
      • Peterson W.F.
      • Berry F.N.
      • Grace M.R.
      • Gulbranson C.L.
      Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
      ,
      • Grimes D.
      • Schulz K.
      • Cates Jr., W.
      Prevention of uterine perforation during curettage abortion.
      ,
      • Schulz K.
      • Grimes D.
      • Cates Jr., W.
      Measures to prevent cervical injury during suction curettage abortion.
      Inadequate cervical dilation
      • Grimes D.
      • Schulz K.
      • Cates Jr., W.
      Prevention of uterine perforation during curettage abortion.
      Non-use of intraoperative ultrasound
      • Darney P.D.
      • Sweet R.L.
      Routine intraoperative ultrasonography for second trimester abortion reduces incidence of uterine perforation.
      Increased gestational age
      • De La Vega G.
      • Nemiroff R.
      • Debbs R.
      Complications of second-trimester dilation and evacuation.
      ,
      • Grimes D.
      • Schulz K.
      • Cates Jr., W.
      Prevention of uterine perforation during curettage abortion.
      Abnormal placentationUterine scar
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      CoagulopathyPersonal or family history of bleeding
      • Goodeve A.
      • Rosén S.
      • Verbruggen B.
      Haemophilia A and von Willebrand's disease.
      Retained tissueIntraoperative ultrasound
      • Acharya G.
      • Morgan H.
      • Paramanantham L.
      • Fernando R.
      A randomized controlled trial comparing surgical termination of pregnancy with and without continuous ultrasound guidance.
      Surgical inexperience
      • Peterson W.F.
      • Berry F.N.
      • Grace M.R.
      • Gulbranson C.L.
      Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
      Perforation, a rare complication of abortion, can be dangerous if it leads to hemorrhage. Estimates of the frequency of perforation vary from 0.1 per 1,000 to 3 per 1,000 [
      • Hakim-Elahi E.
      • Tovell H.M.
      • Burnhill M.S.
      Complications of first-trimester abortion: a report of 170,000 cases.
      ,
      • Choudhary N.
      • Saha S.C.
      • Gopalan S.
      Abortion procedures in a tertiary care institution in India.
      ,
      • Castleman L.D.
      • Oanh K.T.
      • Hyman A.G.
      • Thuy le T.
      • Blumenthal P.D.
      Introduction of the dilation and evacuation procedure for second-trimester abortion in Vietnam using manual vacuum aspiration and buccal misoprostol.
      ,
      • Pridmore B.
      • Chambers D.
      Uterine perforation during surgical abortion: a review of diagnosis, management, and prevention.
      ,
      • De La Vega G.
      • Nemiroff R.
      • Debbs R.
      Complications of second-trimester dilation and evacuation.
      ,
      • Lindell G.
      • Flam F.
      Management of uterine perforations in connection with legal abortions.
      ,
      • Wadhera S.
      Early complication risks of legal abortions, Canada, 1975-1980.
      ] with higher frequencies occurring in training settings and at higher gestational ages [
      • Choudhary N.
      • Saha S.C.
      • Gopalan S.
      Abortion procedures in a tertiary care institution in India.
      ,
      • Castleman L.D.
      • Oanh K.T.
      • Hyman A.G.
      • Thuy le T.
      • Blumenthal P.D.
      Introduction of the dilation and evacuation procedure for second-trimester abortion in Vietnam using manual vacuum aspiration and buccal misoprostol.
      ,
      • Pridmore B.
      • Chambers D.
      Uterine perforation during surgical abortion: a review of diagnosis, management, and prevention.
      ,
      • De La Vega G.
      • Nemiroff R.
      • Debbs R.
      Complications of second-trimester dilation and evacuation.
      ,
      • Grimes D.
      • Schulz K.
      • Cates Jr., W.
      Prevention of uterine perforation during curettage abortion.
      ]. In a study of concurrent laparoscopic sterilization during first-trimester abortion, suspected and actual perforations were two per 1,000 and 15 per 1,000 perforations, respectively, indicating that the true frequency of perforation is likely higher than reported [
      • Kaali S.
      • Szigetvari I.
      • Bartfai G.
      The frequency and management of uterine perforations during first-trimester abortions.
      ]. However, most perforations are small, not clinically significant and effectively managed conservatively. In a prospective study of over 67,000 D&Es, use of osmotic dilators significantly decreased the risk of perforation [
      • Grimes D.
      • Schulz K.
      • Cates Jr., W.
      Prevention of uterine perforation during curettage abortion.
      ]. In a study comparing perforation before and after a clinical policy change, intraoperative ultrasound during D&E was shown to decrease the risk of perforation [
      • Darney P.D.
      • Sweet R.L.
      Routine intraoperative ultrasonography for second trimester abortion reduces incidence of uterine perforation.
      ]. The use of a sound prior to abortion has been associated with increased risk of perforation [
      • Chen L.
      • Lai S.
      • Lee W.
      • Leong N.
      Uterine perforation during elective first trimester abortions: a 13-year review.
      ,
      • White M.
      • Ory H.
      • Goldenberg L.
      A case-control study of uterine perforations documented at laparoscopy.
      ].
      Cervical lacerations are reported to occur in as many as 3% of second-trimester abortions [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ,
      • Ben-Ami I.
      • Schneider D.
      • Svirsky R.
      • Smorgick N.
      • Pansky M.
      • Halperin R.
      Safety of late second-trimester pregnancy termination by laminaria dilatation and evacuation in patients with previous multiple cesarean sections.
      ] and, in most cases, do not lead to hemorrhage [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ]. High, lateral lacerations in the area of the uterine arteries, however, can lead to hemorrhage. Prior cesarean section increases the risk of cervical laceration, with one retrospective study reporting twice as many cervical lacerations (6%) in second-trimester abortion patients with two or more prior cesarean sections [
      • Ben-Ami I.
      • Schneider D.
      • Svirsky R.
      • Smorgick N.
      • Pansky M.
      • Halperin R.
      Safety of late second-trimester pregnancy termination by laminaria dilatation and evacuation in patients with previous multiple cesarean sections.
      ].
      While retained tissue can lead to hemorrhage, most studies examine the association of retained tissue with re-aspiration, not hemorrhage [
      • Patel A.
      • Talmont E.
      • Morfesis J.
      • et al.
      Adequacy and safety of buccal misoprostol for cervical preparation prior to termination of second-trimester pregnancy.
      ,
      • Pridmore B.
      • Chambers D.
      Uterine perforation during surgical abortion: a review of diagnosis, management, and prevention.
      ,
      • Wadhera S.
      Early complication risks of legal abortions, Canada, 1975-1980.
      ]. Because re-aspiration may be done for pain concerning for hematometra, these studies likely overestimate hemorrhage incidence. Re-aspiration is rare, occurring in 0.2–2% of first-trimester abortions [
      • Hakim-Elahi E.
      • Tovell H.M.
      • Burnhill M.S.
      Complications of first-trimester abortion: a report of 170,000 cases.
      ,
      • Wadhera S.
      Early complication risks of legal abortions, Canada, 1975-1980.
      ,

      National Abortion Federation. Summary of abortion statistics. Washington, DC: National Abortion Federation, 1996 [Evidence Grade: III].

      ]. In the second trimester, a suction procedure is more common after medical abortion than surgical abortion [

      Wildschut H, Both MI, Medema S, Thomee E, Wildhagen MF, Kapp N. Medical methods for mid-trimester termination of pregnancy. Cochrane Database Syst Rev:CD005216, 2011 [Evidence Grade: I]

      ], usually for retained placenta and not hemorrhage. Provider inexperience has been associated with retained tissue [
      • Peterson W.F.
      • Berry F.N.
      • Grace M.R.
      • Gulbranson C.L.
      Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
      ].
      Abnormal placentation includes placenta previa as well as placenta accreta, increta and percreta. Although placenta previa has not been associated with postabortion hemorrhage [
      • Thomas A.G.
      • Alvarez M.
      • Friedman Jr., F.
      • Brodman M.L.
      • Kim J.
      • Lockwood C.
      The effect of placenta previa on blood loss in second-trimester pregnancy termination.
      ], placental invasion into and beyond the myometrium can lead to severe hemorrhage. Placenta accreta is estimated to occur in approximately 0.2% of deliveries [
      • Oyelese Y.
      • Smulian J.C.
      Placenta previa, placenta accreta, and vasa previa.
      ], and its incidence continues to rise as cesarean sections become more common.
      Atony, characteristically defined as hypocontractility of the uterine body and fundus, is a common cause of hemorrhage. In a review of nearly 3000 surgical abortions in the second trimester, older maternal age and greater gestational age were identified as independent predictors of atony [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ]. The increased risk of hemorrhage associated with previous cesarean section may be due to atony, with some postulating that the uterine scar impairs the ability of the uterus to contract in a coordinated fashion. While atony of the uterine body or fundus may cause postabortion hemorrhage, lower uterine segment atony has also been described by clinicians after abortion [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ].
      Women who are taking anticoagulants or have bleeding disorders may be at increased risk of bleeding with abortion. Because of this concern, many clinicians discontinue anticoagulants before abortion, a practice that may increase a patient's overall risk, depending on the reason for anticoagulation. A study published in 2011 by Kaneshiro et al. that explored the risk of bleeding with first-trimester abortion among women who continued to take their anticoagulation medications included four women using anticoagulants and six controls. Although mean blood loss was higher in the group taking anticoagulants than among controls (70 mL vs. 22.5 mL), the difference was not clinically significant [
      • Kaneshiro B.
      • Bednarek P.
      • Isley M.
      • Jensen J.
      • Nichols M.
      • Edelman A.
      Blood loss at the time of first-trimester surgical abortion in anticoagulated women.
      ]. The two most common bleeding disorders are von Willebrand disease (VWD) and hemophilia. The prevalence of VWD among women with menorrhagia is as high as 20% [
      • James A.H.
      Women and bleeding disorders.
      ], and in these women, detailed histories of bleeding with procedures, especially deliveries, should be elicited. Other bleeding disorders include platelet dysfunction and factor deficiencies, conditions sufficiently that are rare on a population level.
      Disseminated intravascular coagulopathy (DIC) is a rare complication of abortion and can occur either as a result of hemorrhage or for unknown causes. In cases in which hemorrhage after abortion is not caused by a known etiology, idiopathic DIC should be considered. DIC is characterized by massive activation of the coagulation system, resulting in an imbalance between procoagulant and anticoagulant factors, ultimately producing a hypocoagulable state. In cases of idiopathic DIC, the diagnosis of amniotic fluid embolism (AFE) should be considered. AFE, an exceedingly rare event with an incidence of 3.3 per 100,000 [
      • Roberts C.L.
      • Algert C.S.
      • Knight M.
      • Morris J.M.
      Amniotic fluid embolism in an Australian population-based cohort.
      ], is characterized by a systemic inflammatory response with concomitant cardiovascular collapse and DIC [
      • Clark S.L.
      Amniotic fluid embolism.
      ].

      Treatment of hemorrhage

      Algorithm

      Developing an organized approach is crucial to effectively evaluating and treating postabortion hemorrhage, as we describe in Fig. 2. The first step in the approach to bleeding is a physical exam, of which the three key components are visual and digital inspection of the cervix to identify cervical laceration or perforation, bimanual examination to assess uterine tone, and ultrasound to assess re-accumulation of blood or retained tissue. Some clinicians have found the “cannula test” to be helpful in distinguishing lower uterine segment or high cervical bleeding (e.g., site of a previous scar or cervical laceration) from that of atony at the fundus. The cannula test is done by inserting an 8–10 mm cannula into the fundus and withdrawing it slowly to identify when bleeding through the cannula is briskest.

      Primary treatment

      In many cases, primary treatment measures will be effective and sufficient treatment. If there is a cervical laceration, the location and extent of the laceration should be evaluated through a digital exam and correlated with the recollection of the clinician who performed the abortion procedure. If needed, assistance should be called for in order to obtain optimal visualization. Small lacerations on the face of the cervix may be treated with direct pressure and/or application of silver nitrate. Larger lacerations and lacerations inside the cervix may necessitate ferric subsulfate (Monsel's solution). Surgical repair with absorbable sutures is recommended for external cervical lacerations that are bleeding or are greater than 1 centimeter. If bleeding is persistent after repair of a high cervical tear, one should consider a possible uterine artery laceration.
      In the absence of evidence of a cervical laceration or perforation, uterine massage should be initiated. Often this is done in conjunction with the bimanual exam during the assessment phase. Either during uterine massage or if uterine massage fails to control bleeding, administration of uterotonic therapy is a logical next step. While treatment measures are being employed, it is important to continually return to assessment measures such as bimanual exam and ultrasound, if available, in order to direct the next therapeutic steps.
      Uterotonic agents are a staple of primary treatment, with a retrospective cohort study reporting that 41% of cases of uterine atony were successfully treated with uterotonics alone [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ]. Uterotonics should be administered immediately if massage alone fails. Methylergonovine maleate and misoprostol are commonly used uterotonic medications for postabortion hemorrhage [
      • O'Connell K.
      • Jones H.
      • Simon M.
      • Saporta V.
      • Paul M.
      • Lichtenberg E.
      First-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ,
      • O'Connell K.
      • Jones H.E.
      • Lichtenberg E.S.
      • Paul M.
      Second-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ]; oxytocin and carboprost are less commonly used. Little evidence exists to recommend starting with a particular agent. If the hemorrhage is severe or does not resolve with a single uterotonic agent, additional or repeat doses of uterotonics can be administered.
      Methylergonovine maleate has a rapid onset (within 5 minutes) and, unless contraindicated, is appropriate as a first-line agent to manage postabortion hemorrhage. It can be administered intramuscularly or intravascularly as a 0.2 mg dose. Intramuscular administration is most common. Frequency of dosing is controversial, and in the case of serious hemorrhage, some clinicians repeat the dose every 5 minutes for a maximum of 5 doses. In the absence of evidence, clinical judgment should be exercised in determining the most appropriate dosing schedule.
      Misoprostol is an effective uterotonic in cases of post-abortion hemorrhage, although the route and frequency of dosing are unknown. In the setting of hemorrhage, doses of 800 to 1000 mcg are recommended [

      National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

      ]. The time to peak concentration is most rapid with oral and sublingual administration, though sublingual administration effects the highest serum concentration [
      • Tang O.
      • Schweer H.
      • Seyberth H.
      • Lee S.
      • Ho P.
      Pharmacokinetics of different routes of administration of misoprostol.
      ]. Compared with oral administration, vaginal administration achieves a higher peak concentration [
      • Tang O.
      • Schweer H.
      • Seyberth H.
      • Lee S.
      • Ho P.
      Pharmacokinetics of different routes of administration of misoprostol.
      ] but is usually not feasible in the setting of postabortion hemorrhage. Rectal administration is associated with rapid onset, but lower peak concentration, and lower uterine tone and activity than buccal or vaginal administration [
      • Meckstroth K.
      • Whitaker A.
      • Bertisch S.
      • Goldberg A.
      • Darney P.
      Misoprostol administered by epithelial routes: drug absorption and uterine response.
      ]. On the basis of their pharmacokinetics, sublingual and buccal administration may be preferable to rectal administration.
      Oxytocin is considered an effective uterotonic, but its usefulness in controlling postabortion hemorrhage is unknown and may be lower than that of other uterotonics because a mid-trimester uterus has fewer oxytocin receptors [
      • Hendricks C.H.
      • Berger G.S.
      • Brenner W.E.
      • Keith L.G.
      Second-trimester abortion: perspectives after a decade of experience.
      ]. When used, it is typically given as 10 U intramuscularly or 10 to 40 U intravascularly [

      National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

      ]. Although vasopressin has not been evaluated as a treatment for postabortion hemorrhage, its vasoconstrictive properties may aid in controlling bleeding when administered intracervically or paracervically.

      Secondary treatment

      When bleeding is excessive or refractory to massage and uterotonics, the clinician should move quickly to secondary treatment measures (Fig. 2). The following measures should be instituted without delay: placement of additional intravenous lines, fluid resuscitation and laboratory assessment including hemoglobin, coagulation parameters and a cross-match for possible blood transfusion. It is important to have blood and coagulation factors available in the setting of hemorrhage to properly manage DIC, a potential cause or effect of the hemorrhage. If clinical suspicion of DIC is high, evidenced by a protracted clotting time, treatment with transfusion of red blood cells (RBCs) and fresh frozen plasma (FFP) should be started. Laboratory results will then guide further need for transfusion of RBCs, FFP, cryoprecipitate and platelets. If available, anesthesiologists should be alerted to the possibility of resuscitation needs and surgery. For providers at clinics without immediate availability of anesthesiologists or operating room facilities, it is important to develop clear protocols for resuscitation and transfer to nearby hospitals.
      Re-aspiration is appropriate if there is evidence of retained tissue or re-accumulation of blood on ultrasound. If retained tissue or hematometra is not suspected, and the etiology is thought to be atony or lower uterine segment bleeding, the clinician can consider placement of a Foley or Bakri balloon to tamponade the endometrium. This off-label use of the Foley is supported by a case report from 1995 [
      • Kauff N.D.
      • Chelmow D.
      • Kawada C.Y.
      Intractable bleeding managed with Foley catheter tamponade after dilation and evacuation.
      ] as well as by a retrospective cohort study of second-trimester surgical abortion complications between 2004 and 2007 in which a Foley was used in 37 of 78 patients with hemorrhage from uterine atony [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ]. Once the Foley balloon is proximal to the cervix, it may be inflated to between 30 cc and 80 cc with normal saline (NS). The Bakri balloon was specifically designed for postpartum hemorrhage and may also be used in the postabortion setting. Two case reports from 2007 and 2009 describe successful use of the Bakri in controlling hemorrhage after abortion [
      • Olamijulo J.
      • Doufekas K.
      Intrauterine balloon tamponade for uncontrollable bleeding during first trimester surgical termination of pregnancy.
      ,
      • Madden T.
      • Burke A.
      Successful management of second-trimester postabortion hemorrhage with an intrauterine tamponade balloon.
      ]. Although the Bakri can hold up to 500 cc NS, the two case reports describe inflating the balloon to 250 cc [
      • Olamijulo J.
      • Doufekas K.
      Intrauterine balloon tamponade for uncontrollable bleeding during first trimester surgical termination of pregnancy.
      ] and 120 cc [
      • Madden T.
      • Burke A.
      Successful management of second-trimester postabortion hemorrhage with an intrauterine tamponade balloon.
      ] with successful tamponade. A common strategy is an initial trial of a Foley with 30–40 cc of NS, increasing the volume to 80 cc as needed. These balloons should be filled only with normal saline and never with gas, as this may theoretically lead to an air embolus.
      In cases of hemorrhage requiring transfusion, it is reasonable to leave the balloon in place for 12–24 hours, both for tamponade and while awaiting hemodynamic stability. In cases where balloon tamponade results in rapid hemostasis and the patient is hemodynamically stable, a shorter course of 2–12 hours is often sufficient. While a balloon is in place, the patient should be regularly evaluated for continued bleeding, either around the balloon or through the tubing. Uterotonics may be administered regularly while the balloon is in place (Fig. 2). While there is no evidence on which to make a recommendation regarding antibiotics with the balloon in place, clinicians may want to consider it more in cases of longer placement (12–24 hours) than in cases of shorter placement (2–12 hours). The balloon should be deflated slowly, leaving it in position so that if the bleeding resumes, it can be re-inflated easily.

      Tertiary treatment

      Intensive interventions such as uterine artery embolization (UAE), laparoscopy, laparotomy and hysterectomy may be necessary in the event that primary and secondary treatment measures are unsuccessful in controlling bleeding. UAE as treatment for refractory postabortion hemorrhage has been described in several case series with a total of more than 70 cases [
      • Steinauer J.E.
      • Diedrich J.T.
      • Wilson M.W.
      • Darney P.D.
      • Vargas J.E.
      • Drey E.A.
      Uterine artery embolization in postabortion hemorrhage.
      ,
      • Borgatta L.
      • Chen A.Y.
      • Reid S.K.
      • Stubblefield P.G.
      • Christensen D.D.
      • Rashbaum W.K.
      Pelvic embolization for treatment of hemorrhage related to spontaneous and induced abortion.
      ,
      • Haddad L.
      • Delli-Bovi L.
      Uterine artery embolization to treat hemorrhage following second-trimester abortion by dilatation and surgical evacuation.
      ]. The largest of these series, describing 42 patients who underwent postabortion UAE, reported 100% success in treating refractory hemorrhage from atony, cervical laceration, DIC and lower uterine segment bleeding [
      • Steinauer J.E.
      • Diedrich J.T.
      • Wilson M.W.
      • Darney P.D.
      • Vargas J.E.
      • Drey E.A.
      Uterine artery embolization in postabortion hemorrhage.
      ]. In cases of placenta accreta, UAE was successful in treating 43% of cases (4 of 7 women eventually needed hysterectomy). Two complications of UAE were noted: one contrast reaction treated with diphenhydramine and one femoral embolus requiring emergent embolectomy. Because UAE is associated with less morbidity and mortality than laparotomy and hysterectomy, we recommend attempting UAE prior to more invasive measures in settings where UAE is available. In specific circumstances, UAE can serve as an adjunct treatment with laparotomy. Two cases are described in the literature in which postabortion hemorrhage was initially controlled with UAE, followed by laparotomy [
      • Steinauer J.E.
      • Diedrich J.T.
      • Wilson M.W.
      • Darney P.D.
      • Vargas J.E.
      • Drey E.A.
      Uterine artery embolization in postabortion hemorrhage.
      ]. In one case, a perforation was identified and repaired by laparotomy. In the other case, laparotomy revealed a stable broad ligament hematoma and no perforation.
      If interventional radiology is not available, the next step in treating hemorrhage refractory to primary and secondary measures should be laparotomy. Laparotomy is also indicated in cases of confirmed bowel injury, such as viscera identified in the aspirate or forceps, or in an unstable patient. Laparoscopy may be helpful in confirming a suspected perforation, and when performed by experienced surgeons, can be used to repair a perforation and inspect the bowel. Most often, hemorrhage from a perforation will likely require laparotomy to repair it, and possibly hysterectomy. Though not described in the abortion literature, it is reasonable to attempt to control bleeding with bilateral uterine artery ligation and/or a B-Lynch suture.
      Hysterectomy should be considered only after other treatments have failed. Overall, hysterectomies occur in 1.4 of every 10,000 abortions in the United States [
      • Grimes D.A.
      • Flock M.L.
      • Schulz K.F.
      • Cates Jr., W.
      Hysterectomy as treatment for complications of legal abortion.
      ] and when they do occur, are most often associated with perforation. The decision to proceed to hysterectomy should be made by the clinician by considering the severity of the hemorrhage and the clinician's ability to stabilize the patient with temporizing measures such as transfusion and UAE. Ultimately, hysterectomy is the definitive treatment for postabortion hemorrhage and should be performed rapidly when all other treatments have failed.

      Clinical questions and recommendations

      Which patients are at highest risk for hemorrhage and how can we decrease their risk and prepare to manage them?

      Women at high risk of hemorrhage should be identified preoperatively so that necessary preparations can be made to minimize blood loss. We present an algorithm for identifying and classifying women at risk of hemorrhage from an abortion, with suggestions for directed preparative and preventive techniques according to risk category (Fig. 1). It is important to emphasize that the algorithm is intended as a guide for assessing postabortion hemorrhage risk, but should not be considered prescriptive. Clinical judgment should be exercised when assessing risk. The risk categories were intentionally created with overlap, particularly with respect to history of cesarean sections, to accommodate clinical judgment and variations in clinical resources. Specifically, a clinician may wish to consider a moderate-risk patient high risk, given limitations of the procedure site.
      Figure thumbnail gr1
      Fig. 1Algorithm for classifying women as being at low, moderate or high risk for hemorrhage after abortion.
      Many strategies are used to prevent hemorrhage, but only a few have been studied. In general, efforts should be made to help women obtain an abortion as early as possible in their pregnancy, as morbidity and mortality increase with each additional week of gestation [
      • Bartlett L.A.
      • Berg C.J.
      • Shulman H.B.
      • et al.
      Risk factors for legal induced abortion-related mortality in the United States.
      ]. All women presenting for abortion should have a detailed history, including a review of obstetric complications, and physical examination. Ultrasound confirmation of gestational age is the standard of care [

      National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

      ], as dating by last menstrual period often leads to an underestimate of gestational age, in both the first and the second trimester [
      • Darney P.D.
      • Atkinson E.
      • Hirabayashi K.
      Uterine perforation during second-trimester abortion by cervical dilation and instrumental extraction: a review of 15 cases.
      ,
      • Norman W.V.
      • Bergunder J.
      • Eccles L.
      Accuracy of gestational age estimated by menstrual dating in women seeking abortion beyond nine weeks.
      ]. In order to appropriately assess and manage blood loss, a preoperative hemoglobin or hematocrit level should be obtained for all women undergoing second-trimester abortion, first-trimester medical abortion, and first-trimester surgical abortion if the woman has a history of anemia [

      National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

      ]. A blood type should be obtained for all patients undergoing abortion, as the current standard in the United States is to give anti-D immune globulin for all Rh D-negative patients, even for those at early gestations [

      ACOG practice bulletin. Prevention of Rh D alloimmunization. Number 4, May 1999 (replaces educational bulletin Number 147, October 1990). Clinical management guidelines for obstetrician-gynecologists. American College of Obstetrics and Gynecology. Int J Gynaecol Obstet 1999;66:63-70 [Evidence Grade: III]

      ].
      Prior cesarean sections place women at higher risk of overall complications from second-trimester abortion, with one study demonstrating odds of complications seven times as great among women with two or more cesarean sections as among those with none [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ]. The three most common complications included hemorrhage, atony and cervical laceration. Obesity may be a risk factor for increased blood loss with D&E [
      • Marchiano D.
      • Thomas A.
      • Lapinski R.
      • Balwan K.
      • Patel J.
      Intraoperative blood loss and gestational age at pregnancy termination.
      ,
      • Dark A.
      • Miller L.
      • Kothenbeute R.
      • Mandel L.
      Obesity and second-trimester abortion by dilation and evacuation.
      ], though no well-designed studies have addressed this question. Women with bleeding disorders secondary to either anticoagulation therapy or bleeding diatheses should be identified through a detailed history. Although limited evidence suggests that significant bleeding with first-trimester abortion among anticoagulated patients is not common [
      • Kaneshiro B.
      • Bednarek P.
      • Isley M.
      • Jensen J.
      • Nichols M.
      • Edelman A.
      Blood loss at the time of first-trimester surgical abortion in anticoagulated women.
      ], it may theoretically be more common during second-trimester abortion.
      Although prophylactic uterotonics are used routinely by some providers, available evidence does not support their use. In a National Abortion Federation survey from 2002, providers reported using misoprostol and methylergonovine maleate in both first- and second-trimester abortions [
      • O'Connell K.
      • Jones H.
      • Simon M.
      • Saporta V.
      • Paul M.
      • Lichtenberg E.
      First-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ,
      • O'Connell K.
      • Jones H.E.
      • Lichtenberg E.S.
      • Paul M.
      Second-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ], but the circumstances of their use are unknown. Some clinicians routinely use oxytocin after second-trimester abortion [
      • Marchiano D.
      • Thomas A.
      • Lapinski R.
      • Balwan K.
      • Patel J.
      Intraoperative blood loss and gestational age at pregnancy termination.
      ], although detailed information on its use is limited. One study comparing first-trimester abortion complications before and after use of prophylactic methylergonovine maleate became routine showed a significant decrease in cases of uterine atony and re-aspiration [
      • Sloan N.
      • Durocher J.
      • Aldrich T.
      • Blum J.
      • Winikoff B.
      What measured blood loss tells us about postpartum bleeding: a systematic review.
      ]. Oxytocin does not lead to a significant decrease in blood loss after first-trimester abortion [
      • Lauersen N.
      • Conrad P.
      Effect of oxytocic agents on blood loss during first trimester suction curettage.
      ,
      • Ali P.
      • Smith G.
      The effect of syntocinon on blood loss during first trimester suction curettage.
      ]. No studies have evaluated the prophylactic use of methylergonovine maleate or oxytocin in second-trimester abortions. Randomized, controlled trials of misoprostol in comparison with or in addition to osmotic dilation in the second trimester to evaluate cervical dilation have generally not evaluated blood loss. The few that have done so have found either no difference or a clinically insignificant difference [

      Chitaishvili D, Asatiani T. Sublingual misoprostol prior to manual vacuum aspiration for reducing blood loss at 8-12 weeks of gestation: a randomized double-blind placebo-controlled study. Georgian Med News 2007;26-30 [Evidence Grade: I]

      ,
      • Edelman A.B.
      • Buckmaster J.G.
      • Goetsch M.F.
      • Nichols M.D.
      • Jensen J.T.
      Cervical preparation using laminaria with adjunctive buccal misoprostol before second-trimester dilation and evacuation procedures: a randomized clinical trial.
      ].
      The use of vasopressin in the paracervical block is an intraoperative measure that has been shown to decrease blood loss with D&E [
      • Schulz K.F.
      • Grimes D.A.
      • Christensen D.D.
      Vasopressin reduces blood loss from second-trimester dilatation and evacuation abortion.
      ]. The decreased blood loss associated with vasopressin, demonstrated in a double-blinded, randomized trial, was most pronounced with later gestations [
      • Schulz K.F.
      • Grimes D.A.
      • Christensen D.D.
      Vasopressin reduces blood loss from second-trimester dilatation and evacuation abortion.
      ], and the routine use of vasopressin during D&E is recommended [

      National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

      ]. Use of halogenated anesthetic gases also increases the risk of hemorrhage due to atony, and the use of such agents is now discouraged [
      • Kumarasinghe N.
      • Harpin R.
      • Stewart A.W.
      Blood loss during suction termination of pregnancy with two different anaesthetic techniques.
      ].
      Ultrasound guidance during abortion has been evaluated by two studies. In a randomized, controlled trial in a teaching hospital in the UK, hemorrhage and overall blood loss in cases with ultrasound and in those without were compared [
      • Acharya G.
      • Morgan H.
      • Paramanantham L.
      • Fernando R.
      A randomized controlled trial comparing surgical termination of pregnancy with and without continuous ultrasound guidance.
      ]. Defining hemorrhage as greater than 500 ml blood loss, the study found no difference in hemorrhage with use of ultrasound. Lower blood loss was found with use of ultrasound (103 mL vs. 139 mL), though that difference is likely not clinically significant, despite being statistically significant. Five cases of re-aspiration were reported in the group without ultrasound versus none in the group with ultrasound. Although a provider may wish to use ultrasound during first-trimester abortion, there is no rationale for recommending its routine use [
      • Acharya G.
      • Morgan H.
      • Paramanantham L.
      • Fernando R.
      A randomized controlled trial comparing surgical termination of pregnancy with and without continuous ultrasound guidance.
      ]. The effect of ultrasound guidance on hemorrhage or blood loss with second-trimester abortion is unknown. One study in a training setting has described differences in perforation by comparing cases before and after a policy change made the use of ultrasound routine. To the extent that perforation is associated with the potential for hemorrhage, the results are informative. The study found a decreased perforation rate (0.2% vs. 1.4%) when intraoperative ultrasound was routinely used [
      • Darney P.D.
      • Sweet R.L.
      Routine intraoperative ultrasonography for second trimester abortion reduces incidence of uterine perforation.
      ]. This study, as well, was conducted in a training setting. In a 2002 survey of second-trimester abortion providers, 51% reported that they routinely use ultrasound, with an almost equal proportion using it only for difficult cases [
      • O'Connell K.
      • Jones H.E.
      • Lichtenberg E.S.
      • Paul M.
      Second-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ]. While there are insufficient data to recommend the routine use of ultrasound in second-trimester abortion, clinicians may want to consider its use when multiple passes with forceps (standard D&E) are anticipated, and in training settings.
      The vast majority of patients undergoing first-trimester surgical abortion will be appropriate candidates for an outpatient procedure [
      • Tristan S.B.
      • Gilliam M.
      First trimester surgical abortion.
      ]. Similarly, most second-trimester surgical abortions can be safely completed in the outpatient setting, a practice that is reflected in a survey of second-trimester abortion providers, with only 2% reporting providing services in a hospital-based site [
      • O'Connell K.
      • Jones H.E.
      • Lichtenberg E.S.
      • Paul M.
      Second-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ]. A small proportion of women are at significantly increased risk of hemorrhage, and for these women, strong consideration should be given to referring them to a higher-acuity site. Women with a diagnosis of or concern for placenta accreta (or increta, percreta) or a history of obstetric hemorrhage requiring transfusion should be considered at high risk (Fig. 2), and referral to a high-acuity service is recommended. While most patients in the moderate risk category can be cared for in an outpatient setting, clinicians should be encouraged to use their clinical judgment in deciding whom to refer.
      Figure thumbnail gr2
      Fig. 2Algorithm for a systematic approach to treatment of postabortion hemorrhage.

      Is there evidence that cervical preparation in the second trimester decreases hemorrhage risk?

      Level A evidence supports that routine cervical preparation for surgical abortion at 20–24 weeks decreases procedural risk, likely through decreasing the incidence of cervical laceration, and possibly that of hemorrhage [
      • Frick A.C.
      • Drey E.A.
      • Diedrich J.T.
      • Steinauer J.E.
      Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
      ,
      • Peterson W.F.
      • Berry F.N.
      • Grace M.R.
      • Gulbranson C.L.
      Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
      ,
      • Newmann S.
      • Dalve-Endres A.
      • Drey E.A.
      Clinical guidelines. Cervical preparation for surgical abortion from 20 to 24 weeks' gestation.
      ]. Limited evidence supports specifically recommending osmotic dilators as the best method of cervical preparation for abortions at 20–24 weeks, though current studies are under way to evaluate the efficacy of misoprostol as cervical preparation. Clinical practice varies regarding cervical preparation at 13–20 weeks’ gestation. Same-day preparation with misoprostol or Dilapan-S Dilapan, overnight dilators and a combination of misoprostol and dilators are regimens used for this gestational age range [
      • O'Connell K.
      • Jones H.E.
      • Lichtenberg E.S.
      • Paul M.
      Second-trimester surgical abortion practices: a survey of National Abortion Federation members.
      ]. There is evidence that same-day cervical preparation results in more cases with inadequate cervical dilation [
      • Goldberg A.B.
      • Drey E.A.
      • Whitaker A.K.
      • Kang M.S.
      • Meckstroth K.R.
      • Darney P.D.
      Misoprostol compared with laminaria before early second-trimester surgical abortion: a randomized trial.
      ], but a recent review of 6000 surgical abortions at 12–16 weeks’ gestation with same-day misoprostol cervical ripening reported few complications (three perforations [0.04%] and one case of hemorrhage [0.02%]). Although there is insufficient evidence to recommend one modality for cervical preparation for this gestational age range, there is clinical consensus that any ripening modality is better than none [
      • Grimes D.A.
      • Flock M.L.
      • Schulz K.F.
      • Cates Jr., W.
      Hysterectomy as treatment for complications of legal abortion.
      ,
      • Newmann S.
      • Dalve-Endres A.
      • Drey E.A.
      Clinical guidelines. Cervical preparation for surgical abortion from 20 to 24 weeks' gestation.
      ].

      What diagnostic measures should be taken before abortion when abnormal placentation is suspected?

      Abnormal placentation such as placenta accreta, increta and percreta, characteristically seen in women with a prior uterine scar, has the potential to cause massive hemorrhage during second-trimester surgical abortion [
      • Diedrich J.
      • Steinauer J.
      Complications of surgical abortion.
      ]. Over the past 30 years, the incidence of placenta accreta has increased fourfold, with approximately 3 per 1,000 deliveries affected, largely due to the increased number of cesarean deliveries. In a woman with one prior cesarean section, the risk of placenta accreta increases from 0.03% in the absence of placenta previa to 3.3% in its presence, a 100-fold increase (Table 2) [
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      ]. Other independent risk factors for placenta accreta include advanced maternal age, multiparity, smoking, uterine anomalies (including fibroids) and hypertensive disorders [
      • Belfort M.A.
      Placenta accreta.
      ].
      Table 2Frequency of placenta accreta by number of cesarean sections and presence of placenta previa
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      Cesarean sectionPlacenta previaNo placenta previa
      First3.30.03
      Second110.2
      Third400.1
      Fourth610.8
      Fifth670.8
      Sixth674.7
      When hemorrhage occurs, it is typically seen at the time of placental detachment or removal. Diagnosing accreta preoperatively is associated with significantly decreased blood loss at the time of delivery [
      • Wright J.D.
      • Pri-Paz S.
      • Herzog T.J.
      • et al.
      Predictors of massive blood loss in women with placenta accreta.
      ] and likely at the time of second-trimester abortion. Hemorrhage with first-trimester abortion from placenta accreta is rare; however, prolonged bleeding after first-trimester abortion may be an indication of an undiagnosed placenta increta. Three case reports describe placenta increta diagnosed after patients presented for prolonged bleeding after first-trimester abortion, all treated successfully without hysterectomy, two by embolization [
      • Soleymani M.
      • Srikantha M.
      • Majumdar S.
      • et al.
      Successful use of uterine artery embolisation to treat placenta increta in the first trimester.
      ,
      • Takeda A.
      • Koyama K.
      • Imoto S.
      • Mori M.
      • Nakano T.
      • Nakamura H.
      Conservative management of placenta increta after first trimester abortion by transcatheter arterial chemoembolization: a case report and review of the literature.
      ] and one with hysteroscopic and laparoscopic resection [
      • Wang Y.
      • Su T.
      • Huang W.
      • Weng S.
      Laparoscopic management of placenta increta after late first-trimester dilation and evacuation manifesting as an unusual uterine mass.
      ]. Placental location should be identified in all women with a uterine scar who are presenting for second-trimester abortion, and if a complete previa is seen, detailed evaluation with ultrasound is warranted.
      Ultrasound detection of placenta accreta has improved over time, largely as a result of the use of color Doppler instead of gray-scale [
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      ,
      • Shih J.
      • Palacios Jaraquemada J.
      • Su Y.
      • et al.
      Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
      ]. In a 2009 study of diagnostic criteria for placenta accreta using 3D power Doppler, sensitivity and specificity were as high as 97% and 92%, respectively [
      • Shih J.
      • Palacios Jaraquemada J.
      • Su Y.
      • et al.
      Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
      ]. Several studies have compared the sensitivity and specificity of ultrasound and magnetic resonance imaging (MRI) in diagnosing placenta accreta. One retrospective study examined the diagnostic accuracy among all cases of placenta previa or low-lying placenta with a prior cesarean section or prior myomectomy over 5 years [
      • Warshak C.R.
      • Eskander R.
      • Hull A.D.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      ]. Of the 453 cases sampled, 39 had placenta accreta confirmed by pathologic diagnosis. Ultrasound (gray-scale and color Doppler) correctly identified 30 of the 39 cases and correctly ruled out the diagnosis in 398 of 414 cases, for a sensitivity and specificity of 77% and 96%, respectively. MRI was done in 14 of the 16 cases with false positive ultrasound results, and correctly ruled out the diagnosis. Only one of the nine false-negative cases had evaluation with MRI leading to another false-negative diagnosis. Ultrasound is recommended as the imaging modality for evaluation of placenta accreta. In cases where the diagnosis is uncertain, MRI, where available, should be considered.
      UAE is described in more detail for the management of postabortion hemorrhage, but some have suggested its use preoperatively to decrease blood loss when there is high suspicion for placenta accreta. In a case series in which eight women with suspected accreta were treated with UAE prophylactically, four required hysterectomy [
      • Borgatta L.
      • Chen A.Y.
      • Reid S.K.
      • Stubblefield P.G.
      • Christensen D.D.
      • Rashbaum W.K.
      Pelvic embolization for treatment of hemorrhage related to spontaneous and induced abortion.
      ]. In another case series, one patient with suspected placenta increta received prophylactic UAE and still required subsequent hysterectomy [
      • Steinauer J.E.
      • Diedrich J.T.
      • Wilson M.W.
      • Darney P.D.
      • Vargas J.E.
      • Drey E.A.
      Uterine artery embolization in postabortion hemorrhage.
      ]. Embolization in the emergent setting, where available, may be more successful because bleeding vessels can be directly targeted. Preoperative UAE may be more useful in settings where emergent UAE is not always available, though the decision of when to use it should be made on a case-by-case basis by the clinician.

      What are issues specific to hemorrhage in the setting of medical abortion?

      Medical abortion in both the first and second trimesters is associated with more bleeding than with surgical abortion [
      • Hou S.
      • Chen Q.
      • Zhang L.
      • Fang A.
      • Cheng L.
      Mifepristone combined with misoprostol versus intra-amniotic injection of ethacridine lactate for the termination of second trimester pregnancy: a prospective, open-label, randomized clinical trial.
      ,
      • Niinimaki M.
      • Suhonen S.
      • Mentula M.
      • Hemminki E.
      • Heikinheimo O.
      • Gissler M.
      Comparison of rates of adverse events in adolescent and adult women undergoing medical abortion: population register based study.
      ,
      • Thonneau P.
      • Poirel H.
      • Fougeyrollas B.
      • et al.
      A comparative analysis of fall in haemoglobin following abortions conducted by mifepristone (600 mg) and vacuum aspiration.
      ,
      • von Hertzen H.
      • Piaggio G.
      • Wojdyla D.
      • et al.
      Comparison of vaginal and sublingual misoprostol for second trimester abortion: randomized controlled equivalence trial.
      ]; however, the absolute amount of bleeding with medical abortion is low, and only of clinical importance for patients at increased risk of hemorrhage or pre-existing anemia. Defining hemorrhage after first-trimester medical abortion is more challenging, as blood loss is difficult to estimate. A large retrospective registry study published in 2011 erroneously found that the incidence of hemorrhage after first-trimester medical abortion was 15% [
      • Niinimaki M.
      • Suhonen S.
      • Mentula M.
      • Hemminki E.
      • Heikinheimo O.
      • Gissler M.
      Comparison of rates of adverse events in adolescent and adult women undergoing medical abortion: population register based study.
      ], a number out of proportion to other reports, and reflective of an overly sensitive method of defining hemorrhage. In a large-scale prospective trial of more than 16,000 women undergoing medical abortion, only 0.1% experienced hemorrhage requiring transfusion [
      • Ulmann A.
      • Silvestre L.
      • Chemama L.
      • et al.
      Medical termination of early pregnancy with mifepristone (RU 486) followed by a prostaglandin analogue. Study in 16,369 women.
      ].
      Because medical abortions are unsupervised, women who are anemic may not be ideal candidates. The average drop in hemoglobin is 0.7% [
      • Peyron R.
      • Aubeny E.
      • Targosz V.
      • et al.
      Early termination of pregnancy with mifepristone (RU 486) and the orally active prostaglandin misoprostol.
      ] and most studies of medical abortion excluded women with a hemoglobin under 10 g/dl. Caution should be exercised in offering medical abortion to anemic women, but the threshold of anemia is unclear. Most women undergoing medical abortion will have an uncomplicated course, and the decision to offer medical abortion should be left to the clinician in consultation with the patient. Women who are anticoagulated or have bleeding disorders should be directed toward surgical abortion, which allows their bleeding to be monitored in a more controlled fashion. Counseling women prior to medical abortion is vital to ensure that patients recognize when heavy bleeding is excessive, defined by many clinicians as soaking at least two pads per hour for two consecutive hours [

      Paul M, Lichtenberg ES, Borgatta L, Grimes DA, Stubblefield PG, Creinin MD. Management of Unintended and Abnormal Pregnancy: Comprehensive Abortion Care. Chichester, West Sussex, UK: John Wiley & Sons, Ltd, 2009. p. 376. [Evidence Grade: III]

      ,

      Hatcher RA, Trussell J, Nelson AL, Cates W Jr, Stewart FH, Kowal D. Contraceptive Technology. New York: Ardent Media, Inc. 2008. p. 875 [Evidence Grade: III]

      ]. Compared with surgical treatment of early pregnancy failure, medical treatment is associated with increased bleeding [

      Davis AR, Hendlish SK, Westhoff C et al. Bleeding patterns after misoprostol vs surgical treatment of early pregnancy failure: results from a randomized trial. Am J Obstet Gynecol 2007;196:31 e31-37 [Evidence Grade: I]

      ].
      Hemorrhage associated with second-trimester medical abortion occurs most often in the setting of retained placenta [

      Wildschut H, Both MI, Medema S, Thomee E, Wildhagen MF, Kapp N. Medical methods for mid-trimester termination of pregnancy. Cochrane Database Syst Rev:CD005216, 2011 [Evidence Grade: I]

      ]. In a retrospective review of more than 1000 cases of mid-trimester medical abortions using mifepristone and misoprostol [

      Wildschut H, Both MI, Medema S, Thomee E, Wildhagen MF, Kapp N. Medical methods for mid-trimester termination of pregnancy. Cochrane Database Syst Rev:CD005216, 2011 [Evidence Grade: I]

      ], surgical intervention for a retained placenta was required in 8% of cases [
      • Ashok P.W.
      • Templeton A.
      • Wagaarachchi P.T.
      • Flett G.M.
      Midtrimester medical termination of pregnancy: a review of 1002 consecutive cases.
      ]. Smaller studies have reported both lower [
      • Kapp N.
      • Todd C.S.
      • Yadgarova K.T.
      • et al.
      A randomized comparison of misoprostol to intrauterine instillation of hypertonic saline plus a prostaglandin F2alpha analogue for second-trimester induction termination in Uzbekistan.
      ] and higher incidences of retained placenta [
      • Autry A.M.
      • Hayes E.C.
      • Jacobson G.F.
      • Kirby R.S.
      A comparison of medical induction and dilation and evacuation for second-trimester abortion.
      ,
      • Bryant A.G.
      • Grimes D.A.
      • Garrett J.M.
      • Stuart G.S.
      Second-trimester abortion for fetal anomalies or fetal death: labor induction compared with dilation and evacuation.
      ,
      • Turok D.K.
      • Gurtcheff S.E.
      • Esplin M.S.
      • et al.
      Second trimester termination of pregnancy: a review by site and procedure type.
      ] with similar regimens. Although retained placenta is not an uncommon complication of induction termination in the mid-trimester, associated hemorrhage is still rare. Misoprostol with or without mifepristone is associated with a lower incidence of hemorrhage (1–2%) [
      • von Hertzen H.
      • Piaggio G.
      • Wojdyla D.
      • et al.
      Comparison of vaginal and sublingual misoprostol for second trimester abortion: randomized controlled equivalence trial.
      ,
      • Kapp N.
      • Todd C.S.
      • Yadgarova K.T.
      • et al.
      A randomized comparison of misoprostol to intrauterine instillation of hypertonic saline plus a prostaglandin F2alpha analogue for second-trimester induction termination in Uzbekistan.
      ,
      • Mazouni C.
      • Provensal M.
      • Porcu G.
      • et al.
      Termination of pregnancy in patients with previous cesarean section.
      ] than older induction techniques using intra-amniotic administration of saline, prostaglandin and ethacridine lactate [
      • Hou S.
      • Chen Q.
      • Zhang L.
      • Fang A.
      • Cheng L.
      Mifepristone combined with misoprostol versus intra-amniotic injection of ethacridine lactate for the termination of second trimester pregnancy: a prospective, open-label, randomized clinical trial.
      ,
      • Kapp N.
      • Todd C.S.
      • Yadgarova K.T.
      • et al.
      A randomized comparison of misoprostol to intrauterine instillation of hypertonic saline plus a prostaglandin F2alpha analogue for second-trimester induction termination in Uzbekistan.
      ]. Mifepristone with misoprostol is associated with optimal efficacy, effecting delivery in the shortest time [

      Lohr PA, Hayes JL, Gemzell-Danielsson K. Surgical versus medical methods for second t`rimester induced abortion. Cochrane Database Syst Rev:CD006714, 2008 [Evidence Grade: I]

      ]. More limited data also provide evidence that this regimen is associated with less blood loss.
      Women with complete placenta previa are not candidates for vaginal deliveries at term and are typically considered poor candidates for medical abortions in the second trimester. Low-lying and partial previas do not warrant the same concern and should not be used as a reason to discourage a woman from choosing a medical abortion. In Europe, however, where surgical abortion in the second trimester is very limited, several case series have been reported on women undergoing medical abortion in the setting of a placenta previa. In one report, four of nine women required transfusion and one required a hysterectomy for uncontrolled hemorrhage [
      • Ruano R.
      • Dumez Y.
      • Cabrol D.
      • Dommergues M.
      Second - and third-trimester therapeutic terminations of pregnancy in cases with complete placenta previa-does feticide decrease postdelivery maternal hemorrhage?.
      ]. In another report, one of seven women undergoing medical abortion with gemeprost required a transfusion [
      • Nakayama D.
      • Masuzaki H.
      • Miura K.
      • Hiraki K.
      • Yoshimura S.
      • Ishimaru T.
      Effect of placenta previa on blood loss in second-trimester abortion by labor induction using gemeprost.
      ]. Two studies using feticide before medical abortion in the setting of a placenta previa reported no hemorrhage, but only six and two women were included, respectively [
      • Ruano R.
      • Dumez Y.
      • Cabrol D.
      • Dommergues M.
      Second - and third-trimester therapeutic terminations of pregnancy in cases with complete placenta previa-does feticide decrease postdelivery maternal hemorrhage?.
      ,
      • Borras A.
      • Gomez O.
      • Sanz M.
      • Martinez J.M.
      • Puerto B.
      Feticide followed by mifepristone-misoprostol regimen for midtrimester termination of pregnancy in two cases of complete placenta previa.
      ]. Based on limited evidence, surgical abortion is superior to medical abortion for avoiding hemorrhage in the setting of a placenta previa. In cases where the patient strongly prefers medical abortion or surgical abortion is unavailable, the patient should be counseled as to the increased risk of bleeding and hemorrhage. Feticide prior to medical abortion in the setting of a previa may decrease the risk of hemorrhage, though insufficient evidence exists to make a recommendation.

      What are special issues in the management of fetal demise that should be addressed to decrease hemorrhage?

      There is no evidence that embryonic demise or early pregnancy failure in the first trimester is associated with increased hemorrhage. In one large trial comparing bleeding patterns after surgical versus medical treatment of early pregnancy failure, fewer than 1% of patients (4 of 563) required a blood transfusion, all in the medical management arm [

      Davis AR, Hendlish SK, Westhoff C et al. Bleeding patterns after misoprostol vs surgical treatment of early pregnancy failure: results from a randomized trial. Am J Obstet Gynecol 2007;196:31 e31-37 [Evidence Grade: I]

      ]. Older studies describe an association between second-trimester fetal demise with a retained fetus [

      Pritchard JA. Hematological problems associated with delivery, placental abruption, retained dead fetus and amniotic fluid embolism. Clin Hematol 1973;563–586.

      ] and coagulopathy, with one study reporting that DIC may result in 20–25% of cases when the demised fetus is retained for more than 5 weeks [
      • Pollak L.
      • Schiffer J.
      • Leonov Y.
      • Zaidenstein R.
      Acute subdural hematoma following disseminated intravascular coagulation associated with an obstetric catastrophe.
      ]. Several case reports describe patients with fetal demise who subsequently developed DIC, sometimes associated with amniotic fluid embolism [
      • Ray B.K.
      • Vallejo M.C.
      • Creinin M.D.
      • et al.
      Amniotic fluid embolism with second trimester pregnancy termination: a case report.
      ]. Supporting this are hematologic changes that have been reported in women with fetal demise, including increased thrombin generation and platelet activation [
      • 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.
      ], a possible explanatory mechanism for any association between DIC and fetal demise. A recent study of 242 women undergoing second-trimester abortion examined the effect of fetal demise on maternal morbidity [
      • Edlow A.G.
      • Hou M.Y.
      • Maurer R.
      • Benson C.
      • Delli-Bovi L.
      • Goldberg A.B.
      Uterine evacuation for second-trimester fetal death and maternal morbidity.
      ]. Fetal demise did not increase overall morbidity, but was associated with more transfusions (5.8% vs. 0.8%, p=.07). It is unclear if the results support an association between fetal demise and DIC, and the authors offered no explanation for the finding.
      With more routine use of ultrasound, the occurrence of prolonged, retained fetus after fetal demise is less common. However, the interval between demise and procedure is often unknown. Although there is no evidence to recommend any preoperative measures in cases of fetal demise, some clinicians will obtain a coagulation panel prior to a procedure if the fetus has been retained for several weeks. Clinical judgment should be used in assessing women with fetal demise and their risk of bleeding.

      Conclusions and recommendations

      The following recommendations are based on good and consistent scientific evidence (Level A):
      • 1.
        In women with a uterine scar and a placenta previa at 16 or more weeks’ gestation, an evaluation for placenta accreta is strongly recommended. If a formal radiologic evaluation cannot be done, a provider experienced in ultrasound should evaluate for placenta accreta. Ultrasound is recommended as a first step in evaluating for placenta accreta. If the diagnosis is uncertain, MRI should be considered.
      • 2.
        Bleeding is likely to be greater with medical abortion than with surgical abortion, although the rates of hemorrhage remain low. Counseling regarding surgical and medical methods can address this increased risk of bleeding.
      The following recommendations are based on limited or inconsistent scientific evidence (Level B):
      • 1.
        Obtaining a preoperative hemoglobin or hematocrit in all women undergoing second-trimester abortion and anemic women undergoing first-trimester medical abortion.
      • 2.
        In training settings, the routine use of intraoperative ultrasound may decrease the risk of incomplete abortion with first-trimester surgical abortion and may decrease the risk of perforation with standard D&E.
      • 3.
        Including vasopressin in a paracervical block may decrease blood loss from abortion.
      • 4.
        Balloon tamponade can be an effective intervention for controlling brisk hemorrhage or hemorrhage refractory to massage and uterotonics and should be considered early in the process of bleeding and hemorrhage.
      • 5.
        UAE can effectively control hemorrhage caused by many etiologies. Where available in a timely manner, UAE should be considered before hysterectomy for management of postabortion hemorrhage in patients whose perfusion can be maintained during UAE.
      • 6.
        Uterotonic medications can help control hemorrhage from atony. For actively bleeding patients, methylergonovine maleate, misoprostol and vasopressin are appropriate first-line treatments, with methylergonovine maleate and vasopressin effecting the most rapid response.
      • 7.
        Limited evidence exists for the prophylactic use of methylergonovine maleate prior to first-trimester abortion in reducing the need for re-aspiration.
      The following recommendations are based primarily on consensus or expert opinion (Level C):
      • 1.
        Fetal demise with fetus retained for four or more weeks may be associated with an increased risk of DIC. Obtaining a preoperative coagulation parameter can be considered on an individualized basis, though this has not been studied.
      • 2.
        For women at high risk of hemorrhage, referral to a hospital service or high-acuity center may decrease morbidity.
      • 3.
        Oxytocin can be used as a uterotonic after second-trimester abortion.

      Important questions to be answered

      Although hemorrhage after abortion is rare, it is associated with significant morbidity and mortality. Definitions of hemorrhage across studies are inconsistent, and future research should adopt a consistent definition that is clinically meaningful. Research on methods to decrease the risk of postabortion hemorrhage is warranted, and we highlight three potential areas.
      First, research is needed regarding the prophylactic use of uterotonic medications. Some clinicians routinely use these medications before, during or after the abortion despite the lack of evidence. A randomized, controlled trial with assessment of bleeding outcomes comparing different prophylactic uterotonics would best answer this question.
      Second, the use of ultrasound during abortion should be evaluated. Although most first-trimester abortions done in the United States with high safety and efficacy are not done under ultrasound guidance, limited evidence suggests there may be a benefit to its use, particularly in training settings. There is a greater need to investigate the use of ultrasound in the second trimester, when there is a more significant risk of hemorrhage. This study could be accomplished either through a randomized, controlled trial in a setting where ultrasound is not the standard of care, or a multicenter observational cohort study where ultrasound is the standard of care.
      Third, research studies on the optimal regimen for the delivery of the placenta after second-trimester medical abortion are needed. Medical abortion is associated with a greater risk of bleeding as compared to surgical abortion, and many cases of excess bleeding occur in the setting of retained placenta.

      Sources

      The MEDLINE database was used to identify references published between 1955 and December 2011. The database was searched for the following terms: abortion, hemorrhage, abortion complications, bleeding. Abstracts of all languages were included. The abstracts were reviewed and relevant articles obtained. Citations from these journals were reviewed, as well as contemporary textbooks. PUBMED and Google Scholar were searched in English for publications regarding abortion and contraception. In addition, reference lists of identified manuscripts were searched for any additional studies that might be relevant. We also searched the Cochrane Database of Systematic Reviews.

      Authorship

      These guidelines were prepared by Jennifer Kerns, MD, MPH, and Jody Steinauer, MD, MAS, and reviewed and approved by the Board of the Society of Family Planning.

      Conflict of interest

      Jennifer Kerns, MD, MPH, and Jody Steinauer, MD, MAS, report no significant relationships with industries relative to these guidelines. The Society of Family Planning receives no direct support from pharmaceutical companies or other industries.

      Intended audience

      This guideline is for Society of Family Planning fellows and any other health care professionals involved in the provision of care. This guideline may be of interest to other professional groups that set practice standards for family planning services. The purpose of this document is to review the medical literature on postabortion hemorrhage. This evidence-based review should guide clinicians, although it is not intended to dictate clinical care.

      References

        • Bartlett L.A.
        • Berg C.J.
        • Shulman H.B.
        • et al.
        Risk factors for legal induced abortion-related mortality in the United States.
        Obstet Gynecol. 2004; 103 ([Evidence Grade: II-2]): 729-737
        • Hakim-Elahi E.
        • Tovell H.M.
        • Burnhill M.S.
        Complications of first-trimester abortion: a report of 170,000 cases.
        Obstet Gynecol. 1990; 76 ([Evidence Grade: II-2]): 129-135
      1. Paul M, Lichtenberg ES, Borgatta L, Grimes DA, Stubblefield PG, Creinin MD. Management of Unintended and Abnormal Pregnancy: Comprehensive Abortion Care. Chichester, West Sussex, UK: John Wiley & Sons, Ltd, 2009. p. 376. [Evidence Grade: III]

      2. National Abortion Federation 2011 Clinical Policy Guidelines. [Evidence Grade: III]

        • Chen L.
        • Lai S.
        • Lee W.
        • Leong N.
        Uterine perforation during elective first trimester abortions: a 13-year review.
        Singapore Med J. 1995; 36 ([Evidence Grade: II-2]): 63-67
        • Choudhary N.
        • Saha S.C.
        • Gopalan S.
        Abortion procedures in a tertiary care institution in India.
        Int J Gynaecol Obstet. 2005; 91 ([Evidence Grade: II-3]): 81-86
        • Engbaek J.
        • Bartholdy J.
        • Hjortso N.C.
        Return hospital visits and morbidity within 60 days after day surgery: a retrospective study of 18,736 day surgical procedures.
        Acta Anaesthesiol Scand. 2006; 50 ([Evidence Grade: II-2]): 911-919
        • Niinimaki M.
        • Pouta A.
        • Bloigu A.
        • et al.
        Immediate complications after medical compared with surgical termination of pregnancy.
        Obstet Gynecol. 2009; 114 ([Evidence Grade: II-2]): 795-804
        • Altman A.M.
        • Stubblefield P.G.
        • Schlam J.F.
        • Loberfeld R.
        • Osathanondh R.
        Midtrimester abortion with laminaria and vacuum evacuation on a teaching service.
        J Reprod Med. 1985; 30 ([Evidence Grade: III]): 601-606
        • Castleman L.D.
        • Oanh K.T.
        • Hyman A.G.
        • Thuy le T.
        • Blumenthal P.D.
        Introduction of the dilation and evacuation procedure for second-trimester abortion in Vietnam using manual vacuum aspiration and buccal misoprostol.
        Contraception. 2006; 74 ([Evidence Grade: III]): 272-276
        • Frick A.C.
        • Drey E.A.
        • Diedrich J.T.
        • Steinauer J.E.
        Effect of prior cesarean delivery on risk of second-trimester surgical abortion complications.
        Obstet Gynecol. 2010; 115 ([Evidence Grade: III]): 760-764
        • Patel A.
        • Talmont E.
        • Morfesis J.
        • et al.
        Adequacy and safety of buccal misoprostol for cervical preparation prior to termination of second-trimester pregnancy.
        Contraception. 2006; 73 ([Evidence Grade: II-3]): 420-430
        • Peterson W.F.
        • Berry F.N.
        • Grace M.R.
        • Gulbranson C.L.
        Second-trimester abortion by dilatation and evacuation: an analysis of 11,747 cases.
        Obstet Gynecol. 1983; 62 ([Evidence Grade: II-3]): 185-190
        • Steinauer J.E.
        • Diedrich J.T.
        • Wilson M.W.
        • Darney P.D.
        • Vargas J.E.
        • Drey E.A.
        Uterine artery embolization in postabortion hemorrhage.
        Obstet Gynecol. 2008; 111 ([Evidence Grade: III]): 881-889
        • Pridmore B.
        • Chambers D.
        Uterine perforation during surgical abortion: a review of diagnosis, management, and prevention.
        Aust N Z J Obstet Gynaecol. 1999; 39 ([Evidence Grade: III]): 349-353
        • De La Vega G.
        • Nemiroff R.
        • Debbs R.
        Complications of second-trimester dilation and evacuation.
        Obstet Gynecol. 2007; 109 ([Evidence Grade: II-3]): 21S
        • Lindell G.
        • Flam F.
        Management of uterine perforations in connection with legal abortions.
        Acta Obstet Gynecol Scand. 1995; 74 ([Evidence Grade: II-3]): 373-375
        • Wadhera S.
        Early complication risks of legal abortions, Canada, 1975-1980.
        Can J Public Health. 1982; 73 ([Evidence Grade: II-3]): 396-400
        • Grimes D.
        • Schulz K.
        • Cates Jr., W.
        Prevention of uterine perforation during curettage abortion.
        JAMA. 1984; 251 ([Evidence Grade: II-3]): 2108-2111
        • Kaali S.
        • Szigetvari I.
        • Bartfai G.
        The frequency and management of uterine perforations during first-trimester abortions.
        Am J Obstet Gynecol. 1989; 161 ([Evidence Grade: II-3]): 406-408
        • Darney P.D.
        • Sweet R.L.
        Routine intraoperative ultrasonography for second trimester abortion reduces incidence of uterine perforation.
        J Ultrasound Med. 1989; 8 ([Evidence Grade: II-2]): 71-75
        • White M.
        • Ory H.
        • Goldenberg L.
        A case-control study of uterine perforations documented at laparoscopy.
        Am J Obstet Gynecol. 1977; 129 ([Evidence Grade: II-3]): 623-625
        • Ben-Ami I.
        • Schneider D.
        • Svirsky R.
        • Smorgick N.
        • Pansky M.
        • Halperin R.
        Safety of late second-trimester pregnancy termination by laminaria dilatation and evacuation in patients with previous multiple cesarean sections.
        Am J Obstet Gynecol. 2009; 201 ([Evidence Grade: II-2]): 154 e151-155
      3. National Abortion Federation. Summary of abortion statistics. Washington, DC: National Abortion Federation, 1996 [Evidence Grade: III].

      4. Wildschut H, Both MI, Medema S, Thomee E, Wildhagen MF, Kapp N. Medical methods for mid-trimester termination of pregnancy. Cochrane Database Syst Rev:CD005216, 2011 [Evidence Grade: I]

        • Thomas A.G.
        • Alvarez M.
        • Friedman Jr., F.
        • Brodman M.L.
        • Kim J.
        • Lockwood C.
        The effect of placenta previa on blood loss in second-trimester pregnancy termination.
        Obstet Gynecol. 1994; 84 ([Evidence Grade: II-2]): 58-60
        • Oyelese Y.
        • Smulian J.C.
        Placenta previa, placenta accreta, and vasa previa.
        Obstet Gynecol. 2006; 107 ([Evidence Grade: III]): 927-941
        • Kaneshiro B.
        • Bednarek P.
        • Isley M.
        • Jensen J.
        • Nichols M.
        • Edelman A.
        Blood loss at the time of first-trimester surgical abortion in anticoagulated women.
        Contraception. 2011; 83 ([Evidence Grade: III]): 431-435
        • James A.H.
        Women and bleeding disorders.
        Haemophilia. 2010; 16 ([Evidence Grade: III]): 160-167
        • Roberts C.L.
        • Algert C.S.
        • Knight M.
        • Morris J.M.
        Amniotic fluid embolism in an Australian population-based cohort.
        BJOG. 2010; 117 ([Evidence Grade: II-3]): 1417-1421
        • Clark S.L.
        Amniotic fluid embolism.
        Clin Obstet Gynecol. 2010; 53 ([Evidence Grade: III]): 322-328
        • O'Connell K.
        • Jones H.
        • Simon M.
        • Saporta V.
        • Paul M.
        • Lichtenberg E.
        First-trimester surgical abortion practices: a survey of National Abortion Federation members.
        Contraception. 2009; 79 ([Evidence Grade: III]): 385-392
        • O'Connell K.
        • Jones H.E.
        • Lichtenberg E.S.
        • Paul M.
        Second-trimester surgical abortion practices: a survey of National Abortion Federation members.
        Contraception. 2008; 78 ([Evidence Grade: III]): 492-499
        • Tang O.
        • Schweer H.
        • Seyberth H.
        • Lee S.
        • Ho P.
        Pharmacokinetics of different routes of administration of misoprostol.
        Hum Reprod. 2002; 17 ([Evidence Grade: III]): 332-336
        • Meckstroth K.
        • Whitaker A.
        • Bertisch S.
        • Goldberg A.
        • Darney P.
        Misoprostol administered by epithelial routes: drug absorption and uterine response.
        Obstet Gynecol. 2006; 108 ([Evidence Grade: I]): 582-590
        • Hendricks C.H.
        • Berger G.S.
        • Brenner W.E.
        • Keith L.G.
        Second-trimester abortion: perspectives after a decade of experience.
        John Wright PSG Inc, Boston1981 ([Evidence Grade: III])
        • Kauff N.D.
        • Chelmow D.
        • Kawada C.Y.
        Intractable bleeding managed with Foley catheter tamponade after dilation and evacuation.
        Am J Obstet Gynecol. 1995; 173 ([Evidence Grade: III]): 957-958
        • Olamijulo J.
        • Doufekas K.
        Intrauterine balloon tamponade for uncontrollable bleeding during first trimester surgical termination of pregnancy.
        J Obstet Gynaecol. 2007; 27 ([Evidence Grade: III]): 440-441
        • Madden T.
        • Burke A.
        Successful management of second-trimester postabortion hemorrhage with an intrauterine tamponade balloon.
        Obstet Gynecol. 2009; 113 ([Evidence Grade: III]): 501-503
        • Borgatta L.
        • Chen A.Y.
        • Reid S.K.
        • Stubblefield P.G.
        • Christensen D.D.
        • Rashbaum W.K.
        Pelvic embolization for treatment of hemorrhage related to spontaneous and induced abortion.
        Am J Obstet Gynecol. 2001; 185 ([Evidence Grade: III]): 530-536
        • Haddad L.
        • Delli-Bovi L.
        Uterine artery embolization to treat hemorrhage following second-trimester abortion by dilatation and surgical evacuation.
        Contraception. 2009; 79: 452-455
        • Grimes D.A.
        • Flock M.L.
        • Schulz K.F.
        • Cates Jr., W.
        Hysterectomy as treatment for complications of legal abortion.
        Obstet Gynecol. 1984; 63 ([Evidence Grade: II-2]): 457-462
        • Darney P.D.
        • Atkinson E.
        • Hirabayashi K.
        Uterine perforation during second-trimester abortion by cervical dilation and instrumental extraction: a review of 15 cases.
        Obstet Gynecol. 1990; 5 ([Evidence Grade: III]): 441-444
        • Norman W.V.
        • Bergunder J.
        • Eccles L.
        Accuracy of gestational age estimated by menstrual dating in women seeking abortion beyond nine weeks.
        J Obstet Gynaecol Can. 2011; 33 ([Evidence Grade: III]): 252-257
      5. ACOG practice bulletin. Prevention of Rh D alloimmunization. Number 4, May 1999 (replaces educational bulletin Number 147, October 1990). Clinical management guidelines for obstetrician-gynecologists. American College of Obstetrics and Gynecology. Int J Gynaecol Obstet 1999;66:63-70 [Evidence Grade: III]

        • Marchiano D.
        • Thomas A.
        • Lapinski R.
        • Balwan K.
        • Patel J.
        Intraoperative blood loss and gestational age at pregnancy termination.
        Prim Care Update Ob Gyns. 1998; 5 ([Evidence Grade: II-3]): 204-205
        • Dark A.
        • Miller L.
        • Kothenbeute R.
        • Mandel L.
        Obesity and second-trimester abortion by dilation and evacuation.
        J Reprod Med. 2002; 47 ([Evidence Grade: II-3]): 226-230
        • Sloan N.
        • Durocher J.
        • Aldrich T.
        • Blum J.
        • Winikoff B.
        What measured blood loss tells us about postpartum bleeding: a systematic review.
        BJOG. 2010; 117 ([Evidence Grade: III]): 788-800
        • Lauersen N.
        • Conrad P.
        Effect of oxytocic agents on blood loss during first trimester suction curettage.
        Obstet Gynecol. 1974; 44 ([Evidence Grade: II-2]): 428-433
        • Ali P.
        • Smith G.
        The effect of syntocinon on blood loss during first trimester suction curettage.
        Anesthesia. 1996; 51 ([Evidence Grade: II-2]): 483-485
      6. Chitaishvili D, Asatiani T. Sublingual misoprostol prior to manual vacuum aspiration for reducing blood loss at 8-12 weeks of gestation: a randomized double-blind placebo-controlled study. Georgian Med News 2007;26-30 [Evidence Grade: I]

        • Edelman A.B.
        • Buckmaster J.G.
        • Goetsch M.F.
        • Nichols M.D.
        • Jensen J.T.
        Cervical preparation using laminaria with adjunctive buccal misoprostol before second-trimester dilation and evacuation procedures: a randomized clinical trial.
        Am J Obstet Gynecol. 2006; 194 ([Evidence Grade: I]): 425-430
        • Schulz K.F.
        • Grimes D.A.
        • Christensen D.D.
        Vasopressin reduces blood loss from second-trimester dilatation and evacuation abortion.
        Lancet. 1985; 2 ([Evidence Grade: I]): 353-356
        • Kumarasinghe N.
        • Harpin R.
        • Stewart A.W.
        Blood loss during suction termination of pregnancy with two different anaesthetic techniques.
        Anaesth Intensive Care. 1997; 25 ([Evidence Grade: I]): 48-50
        • Acharya G.
        • Morgan H.
        • Paramanantham L.
        • Fernando R.
        A randomized controlled trial comparing surgical termination of pregnancy with and without continuous ultrasound guidance.
        Eur J Obstet Gynecol Reprod Biol. 2004; 114 ([Evidence Grade: I]): 69-74
        • Tristan S.B.
        • Gilliam M.
        First trimester surgical abortion.
        Clin Obstet Gynecol. 2009; 52 ([Evidence Grade: III]): 151-159
        • Newmann S.
        • Dalve-Endres A.
        • Drey E.A.
        Clinical guidelines. Cervical preparation for surgical abortion from 20 to 24 weeks' gestation.
        Contraception. 2008; 77 ([Evidence Grade: III]): 308-314
        • Goldberg A.B.
        • Drey E.A.
        • Whitaker A.K.
        • Kang M.S.
        • Meckstroth K.R.
        • Darney P.D.
        Misoprostol compared with laminaria before early second-trimester surgical abortion: a randomized trial.
        Obstet Gynecol. 2005; 106 ([Evidence Grade: I]): 234-241
        • Diedrich J.
        • Steinauer J.
        Complications of surgical abortion.
        Clin Obstet Gynecol. 2009; 52 ([Evidence Grade: III]): 205-212
        • Silver R.M.
        • Landon M.B.
        • Rouse D.J.
        • et al.
        Maternal morbidity associated with multiple repeat cesarean deliveries.
        Obstet Gynecol. 2006; 107 ([Evidence Grade: II-2]): 1226-1232
        • Belfort M.A.
        Placenta accreta.
        Am J Obstet Gynecol. 2010; 203 ([Evidence Grade: III]): 430-439
        • Wright J.D.
        • Pri-Paz S.
        • Herzog T.J.
        • et al.
        Predictors of massive blood loss in women with placenta accreta.
        Am J Obstet Gynecol. 2011; 205 ([Evidence Grade: II-2]): 1-6
        • Soleymani M.
        • Srikantha M.
        • Majumdar S.
        • et al.
        Successful use of uterine artery embolisation to treat placenta increta in the first trimester.
        Arch Gynecol Obstet. 2009; 279 ([Evidence Grade: III]): 713-715
        • Takeda A.
        • Koyama K.
        • Imoto S.
        • Mori M.
        • Nakano T.
        • Nakamura H.
        Conservative management of placenta increta after first trimester abortion by transcatheter arterial chemoembolization: a case report and review of the literature.
        Arch Gynecol Obstet. 2010; 281 ([Evidence Grade: III]): 381-386
        • Wang Y.
        • Su T.
        • Huang W.
        • Weng S.
        Laparoscopic management of placenta increta after late first-trimester dilation and evacuation manifesting as an unusual uterine mass.
        J Minim Invasive Gynecol. 2011; 18 ([Evidence Grade: III]): 250-253
        • Finberg H.J.
        • Williams J.W.
        Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
        J Ultrasound Med. 1992; 11 ([Evidence Grade: II-3]): 333-343
        • Shih J.
        • Palacios Jaraquemada J.
        • Su Y.
        • et al.
        Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
        Ultrasound Obstet Gynecol. 2009; 33 ([Evidence Grade: II-3]): 193-203
        • Warshak C.R.
        • Eskander R.
        • Hull A.D.
        • et al.
        Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
        Obstet Gynecol. 2006; 108 ([Evidence Grade: II-3]): 573-581
        • Hou S.
        • Chen Q.
        • Zhang L.
        • Fang A.
        • Cheng L.
        Mifepristone combined with misoprostol versus intra-amniotic injection of ethacridine lactate for the termination of second trimester pregnancy: a prospective, open-label, randomized clinical trial.
        Eur J Obstet Gynecol Reprod Biol. 2010; 151 ([Evidence Grade: I]): 149-153
        • Niinimaki M.
        • Suhonen S.
        • Mentula M.
        • Hemminki E.
        • Heikinheimo O.
        • Gissler M.
        Comparison of rates of adverse events in adolescent and adult women undergoing medical abortion: population register based study.
        BMJ. 2011; 342 ([Evidence Grade: II-2].): d2111
        • Thonneau P.
        • Poirel H.
        • Fougeyrollas B.
        • et al.
        A comparative analysis of fall in haemoglobin following abortions conducted by mifepristone (600 mg) and vacuum aspiration.
        Hum Reprod. 1995; 10 ([Evidence Grade: II-2]): 1512-1515
        • von Hertzen H.
        • Piaggio G.
        • Wojdyla D.
        • et al.
        Comparison of vaginal and sublingual misoprostol for second trimester abortion: randomized controlled equivalence trial.
        Hum Reprod. 2009; 24 ([Evidence Grade: I]): 106-112
        • Ulmann A.
        • Silvestre L.
        • Chemama L.
        • et al.
        Medical termination of early pregnancy with mifepristone (RU 486) followed by a prostaglandin analogue. Study in 16,369 women.
        Acta Obstet Gynecol Scand. 1992; 71 ([Evidence Grade: II-3]): 278-283
        • Peyron R.
        • Aubeny E.
        • Targosz V.
        • et al.
        Early termination of pregnancy with mifepristone (RU 486) and the orally active prostaglandin misoprostol.
        N Engl J Med. 1993; 328 ([Evidence Grade: II-2]): 1509-1513
      7. Hatcher RA, Trussell J, Nelson AL, Cates W Jr, Stewart FH, Kowal D. Contraceptive Technology. New York: Ardent Media, Inc. 2008. p. 875 [Evidence Grade: III]

      8. Davis AR, Hendlish SK, Westhoff C et al. Bleeding patterns after misoprostol vs surgical treatment of early pregnancy failure: results from a randomized trial. Am J Obstet Gynecol 2007;196:31 e31-37 [Evidence Grade: I]

        • Ashok P.W.
        • Templeton A.
        • Wagaarachchi P.T.
        • Flett G.M.
        Midtrimester medical termination of pregnancy: a review of 1002 consecutive cases.
        Contraception. 2004; 69 ([Evidence Grade: III]): 51-58
        • Kapp N.
        • Todd C.S.
        • Yadgarova K.T.
        • et al.
        A randomized comparison of misoprostol to intrauterine instillation of hypertonic saline plus a prostaglandin F2alpha analogue for second-trimester induction termination in Uzbekistan.
        Contraception. 2007; 76 ([Evidence Grade: I]): 461-466
        • Autry A.M.
        • Hayes E.C.
        • Jacobson G.F.
        • Kirby R.S.
        A comparison of medical induction and dilation and evacuation for second-trimester abortion.
        Am J Obstet Gynecol. 2002; 187 ([Evidence Grade: II-2]): 393-397
        • Bryant A.G.
        • Grimes D.A.
        • Garrett J.M.
        • Stuart G.S.
        Second-trimester abortion for fetal anomalies or fetal death: labor induction compared with dilation and evacuation.
        Obstet Gynecol. 2011; 117 ([Evidence Grade: II-2]): 788-792
        • Turok D.K.
        • Gurtcheff S.E.
        • Esplin M.S.
        • et al.
        Second trimester termination of pregnancy: a review by site and procedure type.
        Contraception. 2008; 77 ([Evidence Grade: II-2]): 155-161
        • Mazouni C.
        • Provensal M.
        • Porcu G.
        • et al.
        Termination of pregnancy in patients with previous cesarean section.
        Contraception. 2006; 73 ([Evidence Grade: II-2]): 244-248
      9. Lohr PA, Hayes JL, Gemzell-Danielsson K. Surgical versus medical methods for second t`rimester induced abortion. Cochrane Database Syst Rev:CD006714, 2008 [Evidence Grade: I]

        • Ruano R.
        • Dumez Y.
        • Cabrol D.
        • Dommergues M.
        Second - and third-trimester therapeutic terminations of pregnancy in cases with complete placenta previa-does feticide decrease postdelivery maternal hemorrhage?.
        Fetal Diagn Ther. 2004; 19 ([Evidence Grade: II-3]): 475-478
        • Nakayama D.
        • Masuzaki H.
        • Miura K.
        • Hiraki K.
        • Yoshimura S.
        • Ishimaru T.
        Effect of placenta previa on blood loss in second-trimester abortion by labor induction using gemeprost.
        Contraception. 2007; 75 ([Evidence Grade: II-2]): 238-240
        • Borras A.
        • Gomez O.
        • Sanz M.
        • Martinez J.M.
        • Puerto B.
        Feticide followed by mifepristone-misoprostol regimen for midtrimester termination of pregnancy in two cases of complete placenta previa.
        Fetal Diagn Ther. 2010; 28 ([Evidence Grade: III]): 114-116
      10. Pritchard JA. Hematological problems associated with delivery, placental abruption, retained dead fetus and amniotic fluid embolism. Clin Hematol 1973;563–586.

        • Pollak L.
        • Schiffer J.
        • Leonov Y.
        • Zaidenstein R.
        Acute subdural hematoma following disseminated intravascular coagulation associated with an obstetric catastrophe.
        Isr J Med Sci. 1995; 31 ([Evidence Grade: III]): 489-491
        • Ray B.K.
        • Vallejo M.C.
        • Creinin M.D.
        • et al.
        Amniotic fluid embolism with second trimester pregnancy termination: a case report.
        Can J Anaesth. 2004; 51 ([Evidence Grade: III]): 139-144
        • 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. 1999; 22 ([Evidence Grade: II-2]): 672-687
        • Edlow A.G.
        • Hou M.Y.
        • Maurer R.
        • Benson C.
        • Delli-Bovi L.
        • Goldberg A.B.
        Uterine evacuation for second-trimester fetal death and maternal morbidity.
        Obstet Gynecol. 2011; 117 ([Evidence Grade: II-2]): 307-316
        • Schulz K.
        • Grimes D.
        • Cates Jr., W.
        Measures to prevent cervical injury during suction curettage abortion.
        Lancet. 1983; 1 ([Evidence Grade: II-2]): 1182-1185
        • Goodeve A.
        • Rosén S.
        • Verbruggen B.
        Haemophilia A and von Willebrand's disease.
        Haemophilia. 2010; 5 ([Evidence Grade: III]): 79-84