Hum. Reprod. Advance Access originally published online on March 5, 2008
Human Reproduction 2008 23(5):1087-1092; doi:10.1093/humrep/den049
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Fertility and pregnancy outcomes following uterine devascularization for severe postpartum haemorrhage
Department of Obstetrics and Gynaecology, Rouen University Hospital, Charles Nicolle, 1, rue de Germont, 76031 Rouen-Cedex, France
1 Correspondence address. Tel: +33-2-32-88-82-44; Fax: +33-2-32-88-83-23; E-mail: loicsentilhes{at}hotmail.com
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Abstract |
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BACKGROUND: To evaluate the fertility and pregnancy outcomes following uterine devascularization for postpartum haemorrhage (PPH).
METHODS: All patients who required uterine devascularization, i.e. bilateral uterine artery ligation (Group A), and either bilateral utero-ovarian ligament (Group B) or suspensory ligament of ovary ligation (Group C) in cases of persistent haemorrhage, for PPH with no concomitant procedures from December 1997 to March 2004 were included. Data were retrieved from medical files and telephone interviews.
RESULTS: Data were available for 32 of the 40 (80%) patients included in the study. All patients but 4 had a return to normal menses. Postpartum amenorrhea was secondary to ovarian failure in two cases, and synechiae or necrotic uterus each in one case. These four patients belonged to Group C, whereas no adverse events were observed in groups A and B. Thirteen patients had 16 pregnancies with 13 term deliveries, 1 ectopic pregnancy and 2 abortions. Clinical course of the 13 complete gestations were uneventful but PPH recurred in 4 (31%) due to placenta accreta in three cases.
CONCLUSIONS: Uterine artery ligation, whether or not associated with utero-ovarian ligament ligation, for PPH does not appear to compromise the patients’ subsequent fertility and obstetrical outcome.
Key words: uterine devascularization/postpartum haemorrhage/fertility/pregnancy/uterine artery ligation
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Introduction |
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Severe bleeding is the most significant cause of maternal death worldwide as well as in France (Bouvier-Colle et al., 2001
; AbouZahr, 2003). This is unfortunate because 90% of maternal deaths due to postpartum haemorrhage (PPH) are in fact preventable (Bouvier-Colle et al., 2001). One of the keys to the management of PPH is early stage diagnosis and treatment. In all cases, primary management involves the use of uterotonic agents, manual exploration of the uterus, suturing possible lacerations and fundal massage. In few cases, this primary management remains ineffective and other treatments are required (ACOG Practice Bulletin, 2006), including manual exploration of the uterus, suturing possible lacerations, fundal massage and the use of uterotonic agents such as oxytocin and/or prostaglandin analogues.
The easiest and less morbid procedures should be then preferred (Sergent et al., 2004). In the case of persistent bleeding following vaginal deliveries, pelvic arterial embolization seems to be the ideal procedure only when the patient is haemodynamically stable and the embolization unit is located close to the delivery room (Sergent et al., 2004; ACOG Practice Bulletin, 2006). Moreover, pelvic arterial embolization is limited by the specialized instrumentation and expertise that are required (ACOG Practice Bulletin, 2006). Balloon treatment might be more appropriate following failure of uterotonic agents after vaginal birth (Doumouchtsis et al., 2007). Even if success is incomplete it can at least provide time for performing embolization (Seror et al., 2005; Doumouchtsis et al., 2007). In the case of persistent bleeding following caesarean section, the ideal procedure is the vessel ligation (ACOG Practice Bulletin, 2006).
The first pelvic arteries ligation reported was the hypogastric arteries ligation at the end of the 19th century (Quenu and Duval, 1898). However, many practitioners are only slightly familiar with this technique and the procedure has been found to be considerably less successful than previously thought (Clark et al., 1985; ACOG Practice Bulletin, 2006). Bilateral uterine ligation, as described by O’Leary and O’Leary (1974), accomplishes the same goal and this procedure is quicker and easier to perform (ACOG Practice Bulletin, 2006). As several authors have reported failure of ligation in up to 20% of cases requiring subsequent hysterectomy (Fahmy, 1987), AbdRabbo (1994) subsequently reported a stepwise uterine devascularization procedure, involving normal and low bilateral uterine artery ligation with a bilateral ovarian vessel ligation in cases of persistent haemorrhage. This author reported a hysterectomy avoidance rate of 100% in a 103 case series (AbdRabbo, 1994). Nevertheless, little is known about the fertility and pregnancy outcomes for these patients who have undergone this surgical procedure for severe PPH. This cohort study was therefore undertaken to evaluate the impact on fertility and pregnancy outcomes of stepwise uterine devascularization performed for severe PPH.
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Materials and Methods |
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This study was approved by our Institutional Review Board. All patients who had a stepwise uterine devascularization, as described by AbdRabbo (1994)
, with no concomitant surgical or embolization procedures for severe PPH in our tertiary obstetric hospital (Rouen University Hospital), from December 1997 to March 2004 were included. As previously reported (Sergent et al., 2004), the stepwise uterine devascularization consisted of (i) a bilateral uterine artery ligation followed by a low bilateral uterine artery ligation [i.e. step 3 of the procedure described by AbdRabbo (1994)], (ii) and a bilateral utero-ovarian ligament or suspensory ligament of ovary ligation [i.e. step 5 of the procedure described by AbdRabbo (1994)] only in cases of severe persistent haemorrhage despite the bilateral uterine artery ligation. The suture material used was absorbable sutures (Vicryl 0, Ethicon, France, Neuilly-sur-Seine, France). All the patients who underwent an associated procedure, i.e. primary or secondary pelvic arterial embolization, hypogastric ligation, B-Lynch suture or haemostatic hysterectomy, were excluded from the study. In addition to the stepwise uterine devascularization technique, concomitant therapy, blood transfusion, plasma expanders, antishock measures and fibrinogen were administered depending on the patient’s needs. Our algorithm for management of PPH is shown in Fig. 1 (Sergent et al., 2004). During the study period, 59 pelvic arterial embolizations for primary or secondary PPH were performed.
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The cause and management of the PPH, and the postpartum outcome were retrieved from the hospital records for all patients. During April 2005, in order to have 12 months of minimal follow-up, one of the authors attempted to contact all the patients in this cohort by telephone to determine the mid- and long-term outcome of this procedure. Patients were asked about resumption of menses, menstrual histories, pelvic pain and dyspareunia, modification of sexual function and clinical symptoms of estrogen insufficiency such as hot flushes or vaginal dryness. Finally, patients were also asked about their desire for subsequent pregnancies, attempt to conceive and results. Data regarding the previous and subsequent pregnancies were obtained from the medical records. Descriptive characteristics were calculated for the variables of interest.
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Results |
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During this 9-year period, there were 58 stepwise uterine devascularizations performed in 19 421 deliveries (1 per 335 deliveries). In 3 of the 58 cases (5.2%), PPH occurred after vaginal deliveries. For two of these three cases, as the patient haemodynamics did not allow to perform a pelvic artery embolization, a laparotomy was carried out to control the haemorrhage. Another patient underwent embolization but a laparotomy was required due to persistent haemorrhage. Stepwise uterine devascularization failed to immediately control the haemorrhage in 16 of 58 (27.6%) requiring a subsequent hypogastric ligation in 1 case (1.7%), B-Lynch-suture in 3 cases (5.1%), hypogastric ligation followed by B-Lynch suture in 2 cases (3.4%) and a haemostatic hysterectomy in the remaining 10 cases (17.2%) (Fig. 2). In the failed cases, the cause of the PPH was uterine atony in 8 of 16 (50%), placenta accreta and previa in each 3 of 16 cases (18.8%), and damage of the lower uterine segment in 2 of 16 (12.4%). In one case, stepwise uterine devascularization immediately controlled the haemorrhage; however, pelvic arterial embolization was subsequently performed due to the occurrence of a secondary haemorrhage. Concerning this last case, the cause of primary PPH was uterine atony. After exclusions, the study population consisted of 40 patients (Fig. 2). In our patient population, the stepwise uterine devascularization involved a bilateral uterine artery ligation in 10 of 40 patients (25%) (Group A), a bilateral uterine artery ligation followed by bilateral utero-ovarian ligament ligation in 18 (45%) (Group B) and a bilateral uterine artery ligation followed by bilateral suspensory ligament of ovary ligation in 12 (30%) (Group C).
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Thirty-two of the 40 (80%) patients at follow-up, ranging from 12 to 99 months, were contacted. All the patients belonging to Groups A (n = 9) and B (n = 11) resumed menstruation, whereas in Group C (n = 12), all but 4 (33.3%) resumed menstruation. As regards these four patients, that all belonged to Group C, postpartum amenorrhea was related to (i) a persistence of partial placenta accreta in the uterine cavity leading to a complete synechia in one case (as the patient had no subsequent desire of pregnancy she declined further investigations or operative hysteroscopy), (ii) a hysterectomy in another case due to recurrent pelvic inflammation with no signs of ovarian failure secondary to ischemic and necrotic uterus, that started 15 days after the delivery and was regularly resistant to medical treatment (hysterectomy was performed only 7 months following the delivery as the patient refused a radical treatment several times) (iii) and an ovarian failure confirmed by the hormonal profile in the last two cases. Among the 28 remaining patients, one underwent hysterectomy for micro-invasive cervical cancer. All the other patients considered their menses comparable to that experienced before pregnancy. No patients reported pelvic pain or dyspareunia, change in sexual function, or any reported clinical symptoms of menopause, such as hot flushes or vaginal dryness.
Among the 27 patients where the fertility was preserved (Fig. 2), 11 had no desire for pregnancy. This was due to the fear of PPH recurrence in six cases, and to a cause unrelated to the previous delivery in five cases. In the remaining 16 patients, 4 had been trying to have another child with a median duration of 10 months (range 6–24 months) whereas 12 patients had 16 pregnancies with a mean period until pregnancy (measured from decision to attempted conception) of 6 months (range 2–12 months) for the 14 desired pregnancies. No patient required assisted reproductive procedure. Three of these 16 pregnancies ended during the first trimester of pregnancy: two induced abortions (pregnancies that occurred using oral contraception within the 3 months following the previous delivery) and one ectopic pregnancy treated by salpingectomy.
The characteristics of these subsequent full-term pregnancies are shown in Table I. The patients who had these subsequent pregnancies belonged to Group A in four cases, to Group B in three cases and to Group C in five cases. One patient (patient 11) had two full-term deliveries (cases 11 and 12). In all cases, fetal growth and well-being were assessed by Doppler ultrasound examinations, including uterine and umbilical artery Doppler examination. They were normal in all cases except in one patient with a medical history of chronic hypertension where an intrauterine growth restriction (IUGR) with normal uterine and umbilical Doppler velocimetry was suspected (case 8). These 12 patients gave birth to 13 healthy babies who had all but one (case 8) normal weight for gestational age. Among the three vaginal deliveries, a uterine atony was responsible for a recurrence of PPH in one case that required local procedures (manual removal of placenta, exploration of genital tract, uterine massage) and prostaglandins to stop the haemorrhage (case 7). In the 10 caesarean deliveries, recurrence of PPH occurred in three cases, each time due to placenta accreta (cases 2, 3 and 6). This condition was suspected in two cases due to the presence of placenta previa and by grayscale ultrasound and colour Doppler evaluation of the uteroplacental interface. In one case (case 2), the haemorrhage was controlled by stepwise uterine devascularization, whereas in the two other cases (cases 3 and 6), the first-line surgical treatment of the PPH involved a haemostatic hysterectomy due to previous obstetrical history, the parity and the absence of desire for a future pregnancy.
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Discussion |
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Our results suggest that bilateral uterine artery ligation whether or not associated with bilateral utero-ovarian ligament ligation for PPH does not appear to compromise the patients’ subsequent fertility and obstetrical outcome. We performed a computerized Medline (1966–August 2007) and Embase (1988–August 2007) search, using MeSH terms for ‘stepwise uterine devascularization’, ‘vessel ligation’, ‘postpartum haemorrhage’ and ‘fertility’. The search was not limited by language or publication type (full articles or abstract) and references of retrieved articles were screened. Our results are consistent with those of the only reported study, to our knowledge, in the literature that assessed fertility following stepwise uterine devascularization for the control of PPH (AbdRabbo, 1994
). AbdRabbo (1994) reported, in the 45 patients where follow-up was available, no impact of surgical procedure on the rhythm, duration and amount of menstrual bleeding. Among the 18 patients who stopped contraception, 13 uneventful full-term pregnancies occurred with conception delay at less than 1 year leading to the delivery of 13 normal eutrophic infant live births (AbdRabbo, 1994). Moreover, these results are consistent with those of a dated animal study where no histological changes of the myometrium were observed following bilateral ligation of the uterine and ovarian vessels in dogs (O’Leary, 1980a).
The strengths of this study are the low rate of lost to follow-up (18%) and the number of pregnancies observed in this cohort (16). As regards the 27 patients with a preserved fertility (Fig. 2), no subsequent infertility was observed except for one patient in Group C, who attempted to have another pregnancy during a period of 2 years. In our study, menses resumed early and were unchanged after the surgical procedure. Moreover, no patient who had a desire of future pregnancy required assisted reproductive procedure at the time of the evaluation. No spontaneous abortions occurred and the fetal growth of the 13 full-term pregnancies could be considered normal, as the only case of IUGR was observed in a patient with a chronic arterial hypertension. These pregnancies occurred following bilateral uterine artery ligation alone (Group A) or as well as bilateral utero-ovarian ligament ligation (Group B) or bilateral suspensory ligament of ovary ligation (Group C). PPH recurred in 4 of the 12 deliveries (33.3%), strikingly due to placenta accreta in three cases. These three patients had a previous medical history of caesarean section but no history of abnormal placentation. This high rate of abnormal placentation was also observed in the subsequent pregnancies following pelvic arterial embolization for PPH (Salomon et al., 2003). We therefore hypothesize that a previous devascularized uterus, either by stepwise uterine devascularization or pelvic arterial embolization, might modify implantation and the trophoblast invasion in the subsequent pregnancies, particularly in cases of previous caesarean section. However, one cannot exclude that the high rate of abnormal placentation observed in this situation could simply have been related to the previous deliveries by caesarean section.
Vascular occlusion following stepwise uterine devascularization is suspected to be temporary because recanalization and subsequent normal uterine circulation are expected (AbdRabbo, 1994). It has been suggested that interim collateral circulation may be sufficient to prevent complications (AbdRabbo, 1994). However, in 4 of the 32 (12.5%) patients at follow-up, a severe complication occurred after the stepwise uterine devascularization with bilateral suspensory ligament of ovary ligation. All these four patients belonged to Group C, giving a major complication rate of 33.3% in this group compared with a rate of 0% for Groups A and B. The surgical procedure may clearly be responsible for the two ovarian failure cases, and it cannot be ruled out in the occurrence of the synechiae and in the one case where hysterectomy was required due to an ischemic and necrotic uterus with persistent septic condition. Moreover, we have previously reported a case of ovarian failure and intrauterine synechiae following a stepwise uterine devascularization with both bilateral utero-ovarian ligament and suspensory ligament of ovary ligation which occurred at another center (Roman et al., 2005). These cases must stress that any interruption of ovarian and uterine vascularization is not harmless. In the interest of ovarian vascularization, several authors have proposed bilateral utero-ovarian ligament ligation rather than bilateral suspensory ligament of ovary ligation (Tamizian and Arulkumaran, 2002). It is interesting to note that AbdRabbo (1994) did not observe any complication following bilateral suspensory ligament of ovary ligation and that in our study pregnancies occurred in Group C as well as in Groups A or B. However, considering our high number of complicated cases that occurred only in Group C, we also recommend to prefer bilateral utero-ovarian ligament ligation rather than bilateral suspensory ligament of ovary ligation.
Interestingly, our study emphasizes that women who have a previous medical history of severe PPH are liable to renounce subsequent pregnancy due to the fear of PPH recurrence. This result has been already suggested in two previous reported studies (Nizard et al., 2003; Salomon et al., 2003). Contrary to ours, Salomon et al. (2003) observed that patient who had successful deliveries before this serious complication seemed more likely to want another child. However, as far as we know, this psychological impact of acute obstetrical haemorrhage has never been specifically studied.
To our knowledge, there are only two published studies in the literature that reported pregnancies following bilateral uterine artery ligation to control PPH (O’Leary, 1980b; Fahmy, 1987), whereas this surgical procedure is widely and strongly recommended to control PPH (ACOG Practice Bulletin, 2006). Although limited data are available, these three dated studies document a total of 15 full-term uneventful pregnancies and suggest that this procedure has no effect on the subsequent fertility and the obstetrical outcome (O’Leary, 1980b; Fahmy, 1987). Similarly, there are only few studies that have reported pregnancies following alternative procedures to stepwise uterine devascularization to control PPH, i.e. hypogastric artery ligation, pelvic arterial embolization and B-Lynch-suture (Nizard et al., 2003; Salomon et al., 2003; Descargues et al., 2004; Baskett, 2007). All these studies concluded that each of these procedures did not appear to affect fertility and subsequent obstetrical outcome (Nizard et al., 2003; Salomon et al., 2003; Descargues et al., 2004; Baskett, 2007). Nevertheless, the number of pregnancies was always relatively small as the patients seem to be reluctant to experience a PPH recurrence and take the risk of subsequent pregnancy (Nizard et al., 2003). Furthermore, uterine necrosis and sepsis are now well-known possible outcomes of pelvic artery embolization and B-Lynch suture (Cottier et al., 2002; Ochoa et al., 2002; Pirard et al., 2002; Friederich et al., 2007).
In conclusion, our study confirms that stepwise uterine devascularization for PPH does not appear to compromise the patients’ subsequent fertility and obstetrical outcome. It also suggests that uterine artery ligation associated with suspensory ligament of ovary ligation for PPH should be avoided to control PPH. It further suggests that the risk of abnormal placentation might be increased following a uterine devascularization whatever the procedure used. Additional larger cohort studies are warranted to compare outcome for subsequent pregnancy after stepwise uterine devascularization, hypogastric artery ligation, B-Lynch suture and pelvic arterial embolization to improve conservative management of PPH.
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Author's Role |
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Loïc Sentilhes, Caroline Trichot, Benoit Resch, Horace Roman and Eric Verspyck have participated in analysis and interpretation of data. Caroline Trichot participated in acquisition of data. Loïc Sentilhes, Eric Verspyck and Loïc Marpeau developed the original design. Benoit Resch, Fabrice Sergent, Eric Verspyck and Loïc Marpeau primarily performed the uterine devascularization. Loïc Sentilhes and Eric Verspyck wrote the first draft of the report. All authors contributed to the writing of the final manuscript.
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Acknowledgement |
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The authors are grateful to Richard Medeiros, Rouen University Hospital Medical Editor, for his valuable editorial assistance.
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References |
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Submitted on December 2, 2007; resubmitted on January 24, 2008; accepted on January 31, 2008.
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