Advertisement
JOGC

Guideline No. 430: Diagnosis and management of preterm prelabour rupture of membranes

Published:October 02, 2022DOI:https://doi.org/10.1016/j.jogc.2022.08.014

      Abstract

      Objective

      To provide clear and concise guidelines for the diagnosis and management of preterm prelabour rupture of membranes (PPROM)

      Target Population

      All patients with PPROM <37 weeks gestation

      Benefits, Harms, and Costs

      This guideline aims to provide the first Canadian general guideline on the management of preterm membrane rupture. It includes a comprehensive and up-to-date review of the evidence on the diagnosis, management, timing and method of delivery.

      Evidence

      The following search terms were entered into PubMed/Medline and Cochrane in 2021: preterm premature rupture of membranes, PPROM, chorioamnionitis, Nitrazine test, ferning, commercial tests, placental alpha microglobulin-1 (PAMG-1) test, insulin-like growth factor-binding protein-1 (IGFBP-1) test, ultrasonography, PPROM/antenatal corticosteroids, PPROM/Magnesium sulphate, PPROM/ antibiotic treatment, PPROM/tocolysis, PPROM/preterm labour, PPROM/Neonatal outcomes, PPROM/mortality, PPROM/outpatient/inpatient, PPROM/cerclage, previable PPROM.
      Articles included were randomized controlled trials, meta-analyses, systematic reviews, guidelines, and observational studies. Additional publications were identified from the bibliographies of these articles. Only English-language articles were reviewed.

      Validation Methods

      The authors rated the quality of evidence and strength of recommendations using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach. See Appendix A (Tables A1 for definitions and A2 for interpretations of strong and weak recommendations).

      Intended Audience

      All prenatal and perinatal health care providers.

      SUMMARY STATEMENTS

      • 1.
        Preterm prelabour rupture of membranes complicates approximately 3% of pregnancies and causes approximately one-third of all spontaneous preterm deliveries (high).
      • 2.
        Preterm prelabour rupture of membranes is associated with high neonatal mortality and short- and long-term severe neonatal morbidity such as periventricular leukomalacia, bronchopulmonary dysplasia, necrotizing enterocolitis, retinopathy of prematurity, and adverse neurodevelopment outcomes (high).
      • 3.
        The latency period from rupture of membranes to delivery is negatively correlated with gestational age at preterm prelabour rupture of membranes (high).
      • 4.
        There is insufficient evidence on both the testing modality and the optimal frequency of testing to prevent adverse maternal and perinatal outcomes (low).
      • 5.
        Bed rest is not beneficial in the setting of preterm prelabour rupture of membranes and has adverse maternal effects (high).
      • 6.
        Serial monitoring of white cell count or other markers of inflammation have not been proven to be useful in the absence of other clinical signs of infection (low).
      • 7.
        There is insufficient evidence to recommend hospital versus home management for preterm prelabour rupture of membranes (low).
      • 8.
        Preterm prelabour rupture of membranes may complicate up to 38% of pregnancies in patients who have undergone cervical cerclage (moderate).
      • 9.
        There are no randomized controlled trials comparing different management strategies (or timing) in the setting of previable preterm prelabour rupture of membranes (low).
      • 10.
        Amniotic fluid volume at time of rupture may be helpful in counselling patients and families with previable preterm prelabour rupture of membranes, as anhydramnios and oligohydramnios are more frequently associated with pregnancy loss and pulmonary hypoplasia compared with normal amniotic fluid volumes (low).
      • 11.
        There is conflicting evidence about the relationship between the gestational age at preterm prelabour rupture of membranes in a previous pregnancy and future pregnancy risks (low).
      • 12.
        There is conflicting evidence about the effectiveness of prevention strategies for reducing complications in subsequent pregnancies for patients with a history of preterm prelabour rupture of membranes (moderate).
      • 13.
        The reported recurrence risk of preterm prelabour rupture of membranes in future pregnancy ranges from 10% to 32%, but the most common complication in future pregnancy is preterm birth (34%–46%) (moderate).

      RECOMMENDATIONS

      • 1.
        The diagnosis of preterm prelabour rupture of membranes should be based on the combination of patient’s history and physical examination by a sterile speculum with direct visualization of fluid in the posterior fornix (strong, moderate).
      • 2.
        Digital exam should be avoided to reduce the risk of infection, unless the patient is in active labour (strong, moderate).
      • 3.
        Multiple conventional tests (nitrazine, ferning test, and ultrasound evaluation of amniotic fluid volume) should be considered to confirm the diagnosis of preterm prelabour rupture of membranes when amniotic fluid is not visible at speculum examination (strong, moderate).
      • 4.
        Commercial tests, particularly placental alpha microglobulin-1 (PAMG-1), should be considered following conventional tests in equivocal cases or used as the primary tests in rural and remote areas if other diagnostic options are not available or feasible (strong, moderate).
      • 5.
        Once preterm prelabour rupture of membranes is diagnosed, the initial assessment should include maternal and fetal status with the principal purpose of ruling out active labour, infection (chorioamnionitis), placental abruption, or fetal distress, all conditions that warrant immediate delivery (strong, high).
      • 6.
        Once preterm prelabour rupture of membranes is diagnosed, a vaginal/rectal swab should be obtained to test for group B Streptococcus colonization if not previously done within 5 weeks (conditional, moderate).
      • 7.
        Expectant management with maternal and fetal monitoring should be offered to patients who have no contraindications to continuing the pregnancy (strong, moderate).
      • 8.
        Given that the rate of preterm birth is highest immediately following preterm prelabour rupture of membranes, hospitalization is recommended for the first few days following diagnosis (conditional, low).
      • 9.
        Based on the gestational age at preterm prelabour rupture of membranes and local capacity and resources, antenatal transfer to centres specialized in preterm care should be considered (strong, high).
      • 10.
        The optimal antibiotic regimen for preterm prelabour rupture of membranes remains unclear. If group B Streptococcus status is unknown or positive, the antibiotic regimen should include coverage for this pathogen (strong, moderate).
      • 11.
        The following 2 antibiotic regimens may be used: 1) a macrolide (erythromycin, azithromycin, or clarithromycin) alone or associated with group B Streptococcus coverage for 2 days (if group B Streptococcus status is unknown or positive), or 2) a combination of ampicillin/amoxicillin and a macrolide independently of group B Streptococcus status. There are no data to support extending the antibiotic therapy beyond 10 days (strong, moderate).
      • 12.
        Alternative antibiotic therapy can be considered based on local data on antibiotic resistance (conditional, low).
      • 13.
        Antenatal corticosteroid therapy should be routinely administered to patients with preterm prelabour rupture of membranes at the time of diagnosis when gestational age criteria are met (strong, moderate).
      • 14.
        There is insufficient evidence to support prolonged or recurrent use of tocolysis in the context of preterm prelabour rupture of membranes except for ensuring the full course of corticosteroids for 48 hours, or during transfer to a tertiary care centre in the absence of infection or abruption (conditional, moderate).
      • 15.
        Magnesium sulphate administration for fetal neuroprotection is recommended following preterm prelabour rupture of membranes once the patient is in active labour or prior to indicated delivery, when gestational age criteria are met (strong, moderate).
      • 16.
        If preterm prelabour rupture of membranes occurs before 34 weeks gestation, expectant management with careful monitoring is recommended at least until 35 weeks, in the absence of contraindications, such as infection, placental abruption, cord accident, or abnormal fetal health surveillance. There is conflicting evidence regarding the optimal timing of delivery in cases of preterm prelabour rupture of membranes during the late-preterm period (340 and 366 weeks gestation). If there is evidence of group B Streptococcus colonization, induction of labour should be considered (conditional, moderate).
      • 17.
        In patients with preterm prelabour rupture of membranes and cervical cerclage, there is insufficient evidence on whether the cerclage should be removed or remain in situ. In the absence of signs of infection or other contraindications to retaining a cerclage, either option is reasonable (conditional, low).
      • 18.
        Patients with previable preterm prelabour rupture of membranes should have a consultation with a maternal–fetal medicine specialist and neonatology specialist for comprehensive counselling about prognosis and risks, multidisciplinary management planning, and shared decision-making (conditional, moderate).

      Keywords

      Abbreviations:

      CRP (C-reactive protein), GBS (group B Streptococcus), PPROM (preterm prelabour rupture of the membranes), TVCL (transvaginal cervical length)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Obstetrics and Gynaecology Canada
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Goldenberg R.L.
        • Culhane J.F.
        • Iams J.D.
        • et al.
        Epidemiology and causes of preterm birth.
        Lancet. 2008; 371: 75-84
        • Statistics Canada
        Live births, by weeks of gestation.
        (Available at:)
        • Mercer B.M.
        Preterm premature rupture of the membranes.
        Obstet Gynecol. 2003; 101: 178-193
        • Dammann O.
        • Leviton A.
        • Gappa M.
        • et al.
        Lung and brain damage in preterm newborns, and their association with gestational age, prematurity subgroup, infection/inflammation and long term outcome.
        BJOG. 2005; 11: 4-9
        • Boettcher L.B.
        • Clark E.A.S.
        Neonatal and childhood outcomes following preterm premature rupture of membranes.
        Obstet Gynecol Clin North Am. 2020; 47: 671-680
        • Menon R.
        • Richardson L.S.
        Preterm prelabor rupture of the membranes: a disease of the fetal membranes.
        Semin Perinatol. 2017; 41: 409-419
        • Tchirikov M.
        • Schlabritz-Loutsevitch N.
        • Maher J.
        • et al.
        Mid-trimester preterm premature rupture of membranes (PPROM): etiology, diagnosis, classification, international recommendations of treatment options and outcome.
        J Perinat Med. 2018; 46: 465-488
        • Romero R.
        • Dey S.K.
        • Fisher S.J.
        Preterm labor: one syndrome, many causes.
        Science. 2014; 345: 760-765
        • Romero R.
        • Quintero R.
        • Oyarzun E.
        • et al.
        Intraamniotic infection and the onset of labor in preterm premature rupture of the membranes.
        Am J Obstet Gynecol. 1988; 159: 661-666
        • Rodriguez-Trujillo A.
        • Cobo T.
        • Vives I.
        • et al.
        Gestational age is more important for short-term neonatal outcome than microbial invasion of the amniotic cavity or intra-amniotic inflammation in preterm prelabor rupture of membranes.
        Acta Obstet Gynecol Scand. 2016; 95: 926-933
        • Romero R.
        • Miranda J.
        • Chaemsaithong P.
        • et al.
        Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes.
        J Matern Fetal Neonatal Med. 2015; 28: 1394-1409
        • Musilova I.
        • Kutova R.
        • Pliskova L.
        • et al.
        Intraamniotic inflammation in women with preterm prelabor rupture of membranes.
        PLoS One. 2015; 10e0133929
        • DiGiulio D.B.
        • Romero R.
        • Kusanovic J.P.
        • et al.
        Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes.
        Am J Reprod Immunol. 2010; 64: 38-57
        • Peaceman A.M.
        • Lai Y.
        • Rouse D.J.
        • et al.
        Length of latency with preterm premature rupture of membranes before 32 weeks' gestation.
        Am J Perinatol. 2015; 32: 57-62
        • Melamed N.
        • Hadar E.
        • Ben-Haroush A.
        • et al.
        Factors affecting the duration of the latency period in preterm premature rupture of membranes.
        J Matern Fetal Neonatal Med. 2009; 22: 1051-1056
      1. Prelabor rupture of membranes.
        Obstet Gynecol. 2020; 135: e80-e97
        • Thomson A.J.
        • Royal College of Obstetricians and Gynaecologists
        Care of women presenting with suspected preterm prelabour rupture of membranes from 24(+0) weeks of gestation: green-top guideline no. 73.
        BJOG. 2019; 126: e152-e166
        • Mercer B.M.
        Preterm premature rupture of the membranes: diagnosis and management.
        Clin Perinatol. 2004; 31: 765-782, vi
        • van der Ham D.P.
        • van Teeffelen A.S.
        • Mol B.W.
        Prelabour rupture of membranes: overview of diagnostic methods.
        Curr Opin Obstet Gynecol. 2012; 24: 408-412
        • Alexander J.M.
        • Mercer B.M.
        • Miodovnik M.
        • et al.
        The impact of digital cervical examination on expectantly managed preterm rupture of membranes.
        Am J Obstet Gynecol. 2000; 183: 1003-1007
        • Munson L.A.
        • Graham A.
        • Koos B.J.
        • et al.
        Is there a need for digital examination in patients with spontaneous rupture of the membranes?.
        Am J Obstet Gynecol. 1985; 153: 562-563
        • Seeds A.E.
        • Hellegers A.E.
        Acid-base determinations in human amniotic fluid throughout pregnancy.
        Am J Obstet Gynecol. 1968; 101: 257-260
        • de Haan H.H.
        • Offermans P.M.
        • Smits F.
        • et al.
        Value of the fern test to confirm or reject the diagnosis of ruptured membranes is modest in nonlaboring women presenting with nonspecific vaginal fluid loss.
        Am J Perinatol. 1994; 11: 46-50
        • El-Messidi A.
        • Cameron A.
        Diagnosis of premature rupture of membranes: inspiration from the past and insights for the future.
        J Obstet Gynaecol Can. 2010; 32: 561-569
        • Atlay R.D.
        • Sutherst J.R.
        Premature rupture of the fetal membranes confirmed by intra-amniotic injection of dye (Evans blue T-1824).
        Am J Obstet Gynecol. 1970; 108: 993-994
        • van der Ham D.P.
        • van Melick M.J.
        • Smits L.
        • et al.
        Methods for the diagnosis of rupture of the fetal membranes in equivocal cases: a systematic review.
        Eur J Obstet Gynecol Reprod Biol. 2011; 157: 123-127
        • Palacio M.
        • Kuhnert M.
        • Berger R.
        • et al.
        Meta-analysis of studies on biochemical marker tests for the diagnosis of premature rupture of membranes: comparison of performance indexes.
        BMC Pregnancy Childbirth. 2014; 14: 183
        • Ramsauer B.
        • Vidaeff A.C.
        • Hosli I.
        • et al.
        The diagnosis of rupture of fetal membranes (ROM): a meta-analysis.
        J Perinat Med. 2013; 41: 233-240
        • Sosa C.G.
        • Herrera E.
        • Restrepo J.C.
        • et al.
        Comparison of placental alpha microglobulin-1 in vaginal fluid with intra-amniotic injection of indigo carmine for the diagnosis of rupture of membranes.
        J Perinat Med. 2014; 42: 611-616
        • Smith C.V.
        • Greenspoon J.
        • Phelan J.P.
        • et al.
        Clinical utility of the nonstress test in the conservative management of women with preterm spontaneous premature rupture of the membranes.
        J Reprod Med. 1987; 32: 1-4
        • Liston R.
        • Sawchuck D.
        • Young D.
        No. 197b-fetal health surveillance: intrapartum consensus guideline.
        J Obstet Gynaecol Can. 2018; 40: e298-e322
        • Rizzo G.
        • Capponi A.
        • Angelini E.
        • et al.
        The value of transvaginal ultrasonographic examination of the uterine cervix in predicting preterm delivery in patients with preterm premature rupture of membranes.
        Ultrasound Obstet Gynecol. 1998; 11: 23-29
        • Tsoi E.
        • Fuchs I.
        • Henrich W.
        • et al.
        Sonographic measurement of cervical length in preterm prelabor amniorrhexis.
        Ultrasound Obstet Gynecol. 2004; 24: 550-553
        • Lee S.M.
        • Park K.H.
        • Jung E.Y.
        • et al.
        Frequency and clinical significance of short cervix in patients with preterm premature rupture of membranes.
        PLoS One. 2017; 12e0174657
        • Carlan S.J.
        • Richmond L.B.
        • O'Brien W.F.
        Randomized trial of endovaginal ultrasound in preterm premature rupture of membranes.
        Obstet Gynecol. 1997; 89: 458-461
        • Gire C.
        • Faggianelli P.
        • Nicaise C.
        • et al.
        Ultrasonographic evaluation of cervical length in pregnancies complicated by preterm premature rupture of membranes.
        Ultrasound Obstet Gynecol. 2002; 19: 565-569
        • Mehra S.
        • Amon E.
        • Hopkins S.
        • et al.
        Transvaginal cervical length and amniotic fluid index: can it predict delivery latency following preterm premature rupture of membranes?.
        Am J Obstet Gynecol. 2015; 212 (400.e1–9)
        • Mader J.
        • Craig C.
        Management of group B streptococcus-positive women with preterm premature rupture of the membranes: still a therapeutic dilemma.
        J Obstet Gynaecol Can. 2018; 40: 1627-1631
        • Mercer B.M.
        • Crocker L.G.
        • Boe N.M.
        • et al.
        Induction versus expectant management in premature rupture of the membranes with mature amniotic fluid at 32 to 36 weeks: a randomized trial.
        Am J Obstet Gynecol. 1993; 169: 775-782
        • Goldenberg R.L.
        • Nelson K.G.
        • Davis R.O.
        • et al.
        Delay in delivery: influence of gestational age and the duration of delay on perinatal outcome.
        Obstet Gynecol. 1984; 64: 480-484
        • Sharp G.C.
        • Stock S.J.
        • Norman J.E.
        Fetal assessment methods for improving neonatal and maternal outcomes in preterm prelabour rupture of membranes.
        Cochrane Database Syst Rev. 2014; 10: CD010209
        • Vermillion S.T.
        • Kooba A.M.
        • Soper D.E.
        Amniotic fluid index values after preterm premature rupture of the membranes and subsequent perinatal infection.
        Am J Obstet Gynecol. 2000; 183: 271-276
        • Park J.S.
        • Yoon B.H.
        • Romero R.
        • et al.
        The relationship between oligohydramnios and the onset of preterm labor in preterm premature rupture of membranes.
        Am J Obstet Gynecol. 2001; 184: 459-462
        • Weiner E.
        • Barrett J.
        • Zaltz A.
        • et al.
        Amniotic fluid volume at presentation with early preterm prelabor rupture of membranes and association with severe neonatal respiratory morbidity.
        Ultrasound Obstet Gynecol. 2019; 54: 767-773
        • Mercer B.M.
        • Rabello Y.A.
        • Thurnau G.R.
        • et al.
        The NICHD-MFMU antibiotic treatment of preterm PROM study: impact of initial amniotic fluid volume on pregnancy outcome.
        Am J Obstet Gynecol. 2006; 194: 438-445
        • Gibbs R.S.
        • Duff P.
        Progress in pathogenesis and management of clinical intraamniotic infection.
        Am J Obstet Gynecol. 1991; 164: 1317-1326
        • Etyang A.K.
        • Omuse G.
        • Mukaindo A.M.
        • et al.
        Maternal inflammatory markers for chorioamnionitis in preterm prelabour rupture of membranes: a systematic review and meta-analysis of diagnostic test accuracy studies.
        Syst Rev. 2020; 9: 141
        • van de Laar R.
        • van der Ham D.P.
        • Oei S.G.
        • et al.
        Accuracy of C-reactive protein determination in predicting chorioamnionitis and neonatal infection in pregnant women with premature rupture of membranes: a systematic review.
        Eur J Obstet Gynecol Reprod Biol. 2009; 147: 124-129
        • Trochez-Martinez R.D.
        • Smith P.
        • Lamont R.F.
        Use of C-reactive protein as a predictor of chorioamnionitis in preterm prelabour rupture of membranes: a systematic review.
        BJOG. 2007; 114: 796-801
        • Danesh A.
        • Janghorbani M.
        • Khalatbari S.
        Effects of antenatal corticosteroids on maternal serum indicators of infection in women at risk for preterm delivery: a randomized trial comparing betamethasone and dexamethasone.
        J Res Med Sci. 2012; 17: 911-917
        • Sosa C.G.
        • Althabe F.
        • Belizan J.M.
        • et al.
        Bed rest in singleton pregnancies for preventing preterm birth.
        Cochrane Database Syst Rev. 2015; 3: CD003581
        • Martins I.
        • Pereira I.
        • Clode N.
        A pilot randomized controlled trial of complete bed rest versus activity restriction after preterm premature rupture of the membranes.
        Eur J Obstet Gynecol Reprod Biol. 2019; 240: 325-329
        • Money D.M.
        • Steben M.
        No. 208-guidelines for the management of herpes simplex virus in pregnancy.
        J Obstet Gynaecol Can. 2017; 39: e199-e205
        • Abou El Senoun G.
        • Dowswell T.
        • Mousa H.A.
        Planned home versus hospital care for preterm prelabour rupture of the membranes (PPROM) prior to 37 weeks' gestation.
        Cochrane Database Syst Rev. 2014; 4: CD008053
        • Palmer L.
        • Grabowska K.
        • Burrows J.
        • et al.
        A retrospective cohort study of hospital versus home care for pregnant women with preterm prelabor rupture of membranes.
        Int J Gynaecol Obstet. 2017; 137: 180-184
        • Catt E.
        • Chadha R.
        • Tang S.
        • et al.
        Management of preterm premature rupture of membranes: a comparison of inpatient and outpatient care.
        J Obstet Gynaecol Can. 2016; 38: 433-440
        • Bouchghoul H.
        • Kayem G.
        • Schmitz T.
        • et al.
        Outpatient versus inpatient care for preterm premature rupture of membranes before 34 weeks of gestation.
        Sci Rep. 2019; 9: 4280
        • Kenyon S.
        • Boulvain M.
        • Neilson J.
        Antibiotics for preterm rupture of membranes.
        Cochrane Database Syst Rev. 2003; 12: CD001058
        • Kacerovsky M.
        • Romero R.
        • Stepan M.
        • et al.
        Antibiotic administration reduces the rate of intraamniotic inflammation in preterm prelabor rupture of the membranes.
        Am J Obstet Gynecol. 2020; 223: 114.e1-114.e20
        • Kenyon S.L.
        • Taylor D.J.
        • Tarnow-Mordi W.
        • et al.
        Broad-spectrum antibiotics for preterm, prelabour rupture of fetal membranes: the ORACLE I randomised trial. ORACLE Collaborative Group.
        Lancet. 2001; 357: 979-988
        • Mercer B.M.
        • Miodovnik M.
        • Thurnau G.R.
        • et al.
        Antibiotic therapy for reduction of infant morbidity after preterm premature rupture of the membranes. A randomized controlled trial. National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network.
        JAMA. 1997; 278: 989-995
        • Kenyon S.
        • Pike K.
        • Jones D.R.
        • et al.
        Childhood outcomes after prescription of antibiotics to pregnant women with spontaneous preterm labour: 7-year follow-up of the ORACLE II trial.
        Lancet. 2008; 372: 1319-1327
        • Loeb L.J.
        • Gaither K.
        • Woo K.S.
        • et al.
        Outcomes in gestations between 20 and 25 weeks with preterm premature rupture of membranes.
        South Med J. 2006; 99: 709-712
        • Schrag S.J.
        • Zywicki S.
        • Farley M.M.
        • et al.
        Group B streptococcal disease in the era of intrapartum antibiotic prophylaxis.
        N Engl J Med. 2000; 342: 15-20
        • Stoll B.J.
        • Hansen N.I.
        • Sanchez P.J.
        • et al.
        Early onset neonatal sepsis: the burden of group B Streptococcal and E. coli disease continues.
        Pediatrics. 2011; 127: 817-826
        • Phares C.R.
        • Lynfield R.
        • Farley M.M.
        • et al.
        Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005.
        JAMA. 2008; 299: 2056-2065
        • Weston E.J.
        • Pondo T.
        • Lewis M.M.
        • et al.
        The burden of invasive early-onset neonatal sepsis in the United States, 2005-2008.
        Pediatr Infect Dis J. 2011; 30: 937-941
        • Oh K.J.
        • Romero R.
        • Park J.Y.
        • et al.
        The earlier the gestational age, the greater the intensity of the intra-amniotic inflammatory response in women with preterm premature rupture of membranes and amniotic fluid infection by Ureaplasma species.
        J Perinat Med. 2019; 47: 516-527
        • Lal C.V.
        • Xu X.
        • Jackson P.
        • et al.
        Ureaplasma infection-mediated release of matrix metalloproteinase-9 and PGP: a novel mechanism of preterm rupture of membranes and chorioamnionitis.
        Pediatr Res. 2017; 81: 75-79
        • Navathe R.
        • Schoen C.N.
        • Heidari P.
        • et al.
        Azithromycin vs erythromycin for the management of preterm premature rupture of membranes.
        Am J Obstet Gynecol. 2019; 221: 144.e1-144.e8
        • Pierson R.C.
        • Gordon S.S.
        • Haas D.M.
        A retrospective comparison of antibiotic regimens for preterm premature rupture of membranes.
        Obstet Gynecol. 2014; 124: 515-519
        • Finneran M.M.
        • Smith D.D.
        • Buhimschi C.S.
        Cost analysis of azithromycin versus erythromycin in pregnancies complicated by preterm premature rupture of membranes.
        Am J Perinatol. 2019; 36: 105-110
        • Finneran M.M.
        • Appiagyei A.
        • Templin M.
        • et al.
        Comparison of azithromycin versus erythromycin for prolongation of latency in pregnancies complicated by preterm premature rupture of membranes.
        Am J Perinatol. 2017; 34: 1102-1107
        • Seaman R.D.
        • Kopkin R.H.
        • Turrentine M.A.
        Erythromycin versus azithromycin for treatment of preterm prelabor rupture of membranes: a systematic review and meta-analysis.
        Am J Obstet Gynecol. 2022; 226: 794-801.e1
        • Wolf M.F.
        • Sgayer I.
        • Miron D.
        • et al.
        A novel extended prophylactic antibiotic regimen in preterm pre-labor rupture of membranes: a randomized trial.
        Int J Infect Dis. 2020; 96: 254-259
        • Money D.M.
        • Dobson S.
        • Canadian Paediatric Society IDC
        The prevention of early-onset neonatal group B streptococcal disease.
        J Obstet Gynaecol Can. 2004; 26: 826-840
      2. Ronzoni S, Cobo T, D'Souza R, et al. Individualized treatment of preterm PROM to prolong the latency period, reduce the rate of preterm birth, and improve neonatal outcomes [e-pub ahead of print]. Am J Obstet Gynecol https://doi.org/10.1016/j.ajog.2022.02.037, accessed July 25, 2022.

        • Skoll A.
        • Boutin A.
        • Bujold E.
        • et al.
        No. 364-antenatal corticosteroid therapy for improving neonatal outcomes.
        J Obstet Gynaecol Can. 2018; 40: 1219-1239
        • Roberts D.
        • Brown J.
        • Medley N.
        • et al.
        Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth.
        Cochrane Database Syst Rev. 2017; 3: CD004454
      3. Smith J, Murphy KE, McDonald SD, et al. Timing of antenatal corticosteroids in relation to clinical indication [e-pub ahead of print]. Arch Gynecol Obstet https://doi.org/10.1007/s00404-021-06362-7, accessed July 25, 2022.

        • Magann E.F.
        • Haram K.
        • Ounpraseuth S.
        • et al.
        Use of antenatal corticosteroids in special circumstances: a comprehensive review.
        Acta Obstet Gynecol Scand. 2017; 96: 395-409
        • Fox N.S.
        • Gelber S.E.
        • Kalish R.B.
        • et al.
        Contemporary practice patterns and beliefs regarding tocolysis among U.S. maternal-fetal medicine specialists.
        Obstet Gynecol. 2008; 112: 42-47
        • Mackeen A.D.
        • Seibel-Seamon J.
        • Muhammad J.
        • et al.
        Tocolytics for preterm premature rupture of membranes.
        Cochrane Database Syst Rev. 2014; : CD007062
        • Nijman T.A.
        • van Vliet E.O.
        • Naaktgeboren C.A.
        • et al.
        Nifedipine versus placebo in the treatment of preterm prelabor rupture of membranes: a randomized controlled trial: assessment of perinatal outcome by use of tocolysis in early labor-APOSTEL IV trial.
        Eur J Obstet Gynecol Reprod Biol. 2016; 205: 79-84
        • Lorthe E.
        • Goffinet F.
        • Marret S.
        • et al.
        Tocolysis after preterm premature rupture of membranes and neonatal outcome: a propensity-score analysis.
        Am J Obstet Gynecol. 2017; 217: 212.e1-212.e12
        • Horton A.L.
        • Lai Y.
        • Rouse D.J.
        • et al.
        Effect of magnesium sulfate administration for neuroprotection on latency in women with preterm premature rupture of membranes.
        Am J Perinatol. 2015; 32: 387-392
        • Kamyar M.
        • Manuck T.A.
        • Stoddard G.J.
        • et al.
        Magnesium sulfate, chorioamnionitis, and neurodevelopment after preterm birth.
        BJOG. 2016; 123: 1161-1166
        • Magee L.A.
        • De Silva D.A.
        • Sawchuck D.
        • et al.
        No. 376-magnesium sulphate for fetal neuroprotection.
        J Obstet Gynaecol Can. 2019; 41: 505-522
        • Doyle L.W.
        • Crowther C.A.
        • Middleton P.
        • et al.
        Magnesium sulphate for women at risk of preterm birth for neuroprotection of the fetus.
        Cochrane Database Syst Rev. 2009; 1: CD004661
        • Wolf H.T.
        • Huusom L.D.
        • Henriksen T.B.
        • et al.
        Magnesium sulphate for fetal neuroprotection at imminent risk for preterm delivery: a systematic review with meta-analysis and trial sequential analysis.
        BJOG. 2020; 127: 1180-1188
        • Clark E.A.
        • Varner M.
        Impact of preterm PROM and its complications on long-term infant outcomes.
        Clin Obstet Gynecol. 2011; 54: 358-369
        • Bond D.M.
        • Middleton P.
        • Levett K.M.
        • et al.
        Planned early birth versus expectant management for women with preterm prelabour rupture of membranes prior to 37 weeks' gestation for improving pregnancy outcome.
        Cochrane Database Syst Rev. 2017; 3Cd004735
        • Pasquier J.C.
        • Claris O.
        • Rabilloud M.
        • et al.
        Intentional early delivery versus expectant management for preterm premature rupture of membranes at 28-32 weeks' gestation: a multicentre randomized controlled trial (MICADO STUDY).
        Eur J Obstet Gynecol Reprod Biol. 2019; 233: 30-37
        • Quist-Nelson J.
        • de Ruigh A.A.
        • Seidler A.L.
        • et al.
        Immediate delivery compared with expectant management in late preterm prelabor rupture of membranes: an individual participant data meta-analysis.
        Obstet Gynecol. 2018; 131: 269-279
        • van der Ham D.P.
        • Nijhuis J.G.
        • Mol B.W.
        • et al.
        Induction of labour versus expectant management in women with preterm prelabour rupture of membranes between 34 and 37 weeks (the PPROMEXIL-trial).
        BMC Pregnancy Childbirth. 2007; 7: 11
        • van der Ham D.P.
        • van der Heyden J.L.
        • Opmeer B.C.
        • et al.
        Management of late-preterm premature rupture of membranes: the PPROMEXIL-2 trial.
        Am J Obstet Gynecol. 2012; 207 (276.e1–10)
        • Morris J.M.
        • Roberts C.L.
        • Bowen J.R.
        • et al.
        Immediate delivery compared with expectant management after preterm pre-labour rupture of the membranes close to term (PPROMT trial): a randomised controlled trial.
        Lancet. 2016; 387: 444-452
        • van der Heyden J.L.
        • Willekes C.
        • van Baar A.L.
        • et al.
        Behavioural and neurodevelopmental outcome of 2-year-old children after preterm premature rupture of membranes: follow-up of a randomised clinical trial comparing induction of labour and expectant management.
        Eur J Obstet Gynecol Reprod Biol. 2015; 194: 17-23
        • Tajik P.
        • van der Ham D.P.
        • Zafarmand M.H.
        • et al.
        Using vaginal group B Streptococcus colonisation in women with preterm premature rupture of membranes to guide the decision for immediate delivery: a secondary analysis of the PPROMEXIL trials.
        BJOG. 2014; 121 (discussion 73): 1263-1272
      4. Evidence review for timing of delivery to reduce the risk of early-onset neonatal infection: neonatal infection: antibiotics for prevention and treatment. London: NICE Evidence Reviews Collection; 2021.
        (Available at:)
        • Treadwell M.C.
        • Bronsteen R.A.
        • Bottoms S.F.
        Prognostic factors and complication rates for cervical cerclage: a review of 482 cases.
        Am J Obstet Gynecol. 1991; 165: 555-558
        • Galyean A.
        • Garite T.J.
        • Maurel K.
        • et al.
        Removal versus retention of cerclage in preterm premature rupture of membranes: a randomized controlled trial.
        Am J Obstet Gynecol. 2014; 211 (399.e1–7)
        • Pergialiotis V.
        • Gkioka E.
        • Bakoyiannis I.
        • et al.
        Retention of cervical cerclage after preterm premature rupture of the membranes: a critical appraisal.
        Arch Gynecol Obstet. 2015; 291: 745-753
        • Walsh J.
        • Allen V.M.
        • Colford D.
        • et al.
        Preterm prelabour rupture of membranes with cervical cerclage: a review of perinatal outcomes with cerclage retention.
        J Obstet Gynaecol Can. 2010; 32: 448-452
        • Giraldo-Isaza M.A.
        • Berghella V.
        Cervical cerclage and preterm PROM.
        Clin Obstet Gynecol. 2011; 54: 313-320
        • Vitner D.
        • Melamed N.
        • Elhadad D.
        • et al.
        Removal vs. retention of cervical cerclage in pregnancies complicated by preterm premature rupture of membranes: a retrospective study.
        Arch Gynecol Obstet. 2020; 302: 603-609
        • Ladhani N.N.N.
        • Chari R.S.
        • Dunn M.S.
        • et al.
        No. 347-obstetric management at borderline viability.
        J Obstet Gynaecol Can. 2017; 39: 781-791
        • Linehan L.A.
        • Walsh J.
        • Morris A.
        • et al.
        Neonatal and maternal outcomes following midtrimester preterm premature rupture of the membranes: a retrospective cohort study.
        BMC Pregnancy Childbirth. 2016; 16: 25
        • Gunes A.
        • Kiyak H.
        • Yuksel S.
        • et al.
        Predicting previable preterm premature rupture of membranes (pPPROM) before 24 weeks: maternal and fetal/neonatal risk factors for survival.
        J Obstet Gynaecol. 2022; 42: 597-606
        • Pylypjuk C.
        • Majeau L.
        Perinatal outcomes and influence of amniotic fluid volume following previable, preterm prelabor rupture of membranes (pPPROM): a historical cohort study.
        Int J Womens Health. 2021; 13: 627-637
        • Kibel M.
        • Asztalos E.
        • Barrett J.
        • et al.
        Outcomes of pregnancies complicated by preterm premature rupture of membranes between 20 and 24 weeks of gestation.
        Obstet Gynecol. 2016; 128: 313-320
        • Storness-Bliss C.
        • Metcalfe A.
        • Simrose R.
        • et al.
        Correlation of residual amniotic fluid and perinatal outcomes in periviable preterm premature rupture of membranes.
        J Obstet Gynaecol Can. 2012; 34: 154-158
        • Waters T.P.
        • Mercer B.M.
        The management of preterm premature rupture of the membranes near the limit of fetal viability.
        Am J Obstet Gynecol. 2009; 201: 230-240
        • Kiver V.
        • Boos V.
        • Thomas A.
        • et al.
        Perinatal outcomes after previable preterm premature rupture of membranes before 24 weeks of gestation.
        J Perinat Med. 2018; 46: 555-565
        • Vergani P.
        • Ghidini A.
        • Locatelli A.
        • et al.
        Risk factors for pulmonary hypoplasia in second-trimester premature rupture of membranes.
        Am J Obstet Gynecol. 1994; 170: 1359-1364
        • Rotschild A.
        • Dison P.J.
        • Chitayat D.
        • et al.
        Midfacial hypoplasia associated with long-term intubation for bronchopulmonary dysplasia.
        Am J Dis Child. 1990; 144: 1302-1306
        • Roberts D.
        • Vause S.
        • Martin W.
        • et al.
        Amnioinfusion in very early preterm prelabor rupture of membranes (AMIPROM): pregnancy, neonatal and maternal outcomes in a randomized controlled pilot study.
        Ultrasound Obstet Gynecol. 2014; 43: 490-499
        • van Kempen L.E.M.
        • van Teeffelen A.S.
        • de Ruigh A.A.
        • et al.
        Amnioinfusion compared with no intervention in women with second-trimester rupture of membranes: a randomized controlled trial.
        Obstet Gynecol. 2019; 133: 129-136
        • Smith G.
        • Rafuse C.
        • Anand N.
        • et al.
        Prevalence, management, and outcomes of preterm prelabour rupture of the membranes of women in Canada.
        J Obstet Gynaecol Can. 2005; 27: 547-553
        • van der Heyden J.L.
        • van Kuijk S.M.
        • van der Ham D.P.
        • et al.
        Subsequent pregnancy after preterm prelabor rupture of membranes before 27 weeks' gestation.
        AJP Rep. 2013; 3: 113-118
        • Lee T.
        • Carpenter M.W.
        • Heber W.W.
        • et al.
        Preterm premature rupture of membranes: risks of recurrent complications in the next pregnancy among a population-based sample of gravid women.
        Am J Obstet Gynecol. 2003; 188: 209-213
        • Asrat T.
        • Lewis D.F.
        • Garite T.J.
        • et al.
        Rate of recurrence of preterm premature rupture of membranes in consecutive pregnancies.
        Am J Obstet Gynecol. 1991; 165: 1111-1115
        • Monson M.A.
        • Gibbons K.J.
        • Esplin M.S.
        • et al.
        Pregnancy outcomes in women with a history of previable, preterm prelabor rupture of membranes.
        Obstet Gynecol. 2016; 128: 976-982
        • Macones G.A.
        • Parry S.
        • Elkousy M.
        • et al.
        A polymorphism in the promoter region of TNF and bacterial vaginosis: preliminary evidence of gene-environment interaction in the etiology of spontaneous preterm birth.
        Am J Obstet Gynecol. 2004; 190 (discussion 3A): 1504-1508
        • Friedman M.L.
        • McElin T.W.
        Diagnosis of ruptured fetal membranes. Clinical study and review of the literature.
        Am J Obstet Gynecol. 1969; 104: 544-550
        • Gorodeski I.G.
        • Haimovitz L.
        • Bahari C.M.
        Reevaluation of the pH, ferning and nile blue sulphate staining methods in pregnant women with premature rupture of the fetal membranes.
        J Perinat Med. 1982; 10: 286-292
        • Erdemoglu E.
        • Mungan T.
        Significance of detecting insulin-like growth factor binding protein-1 in cervicovaginal secretions: comparison with nitrazine test and amniotic fluid volume assessment.
        Acta Obstet Gynecol Scand. 2004; 83: 622-626
        • Khooshideh M.
        • Radi V.
        • Hosseini R.
        • et al.
        The accuracy of placental alpha-microglobuline-1 test in diagnosis of premature rupture of the membranes.
        Iran J Reprod Med. 2015; 13: 355-360
        • Liang D.K.
        • Qi H.B.
        • Luo X.
        • et al.
        Comparative study of placental alpha-microglobulin-1, insulin-like growth factor binding protein-1 and nitrazine test to diagnose premature rupture of membranes: a randomized controlled trial.
        J Obstet Gynaecol Res. 2014; 40: 1555-1560
        • Albayrak M.
        • Ozdemir I.
        • Koc O.
        • et al.
        Comparison of the diagnostic efficacy of the two rapid bedside immunoassays and combined clinical conventional diagnosis in prelabour rupture of membranes.
        Eur J Obstet Gynecol Reprod Biol. 2011; 158: 179-182
        • Elci E.
        • Gunes Elci G.
        • Sayan S.
        Comparison of the accuracy and reliability of the AmniSure, AMNIOQUICK, and AL-SENSE tests for early diagnosis of premature rupture of membranes.
        Int J Gynaecol Obstet. 2020; 149: 93-97
        • Eleje G.U.
        • Ezugwu E.C.
        • Eke A.C.
        • et al.
        Diagnostic performance of placental alpha-microglobulin-1 test in women with prolonged pre-labour rupture of membranes.
        J Matern Fetal Neonatal Med. 2016; 29: 1291-1296
        • Galletta M.A.K.
        • Bittar R.E.
        • Rodrigues A.S.
        • et al.
        Comparative analysis of insulin-like growth factor binding protein-1, placental alpha-microglobulin-1, phenol and pH for the diagnosis of preterm premature rupture of membranes between 20 and 36 weeks.
        J Obstet Gynaecol Res. 2019; 45: 1448-1457
        • Shahin M.
        • Raslan H.
        Comparative study of three amniotic fluid markers in premature rupture of membranes: prolactin, beta subunit of human chorionic gonadotropin, and alpha-fetoprotein.
        Gynecol Obstet Invest. 2007; 63: 195-199
        • Buyukbayrak E.E.
        • Turan C.
        • Unal O.
        • et al.
        Diagnostic power of the vaginal washing-fluid prolactin assay as an alternative method for the diagnosis of premature rupture of membranes.
        J Matern Fetal Neonatal Med. 2004; 15: 120-125
        • Kafali H.
        • Oksuzler C.
        Vaginal fluid urea and creatinine in diagnosis of premature rupture of membranes.
        Arch Gynecol Obstet. 2007; 275: 157-160
        • Gezer C.
        • Ekin A.
        • Golbasi C.
        • et al.
        Use of urea and creatinine levels in vaginal fluid for the diagnosis of preterm premature rupture of membranes and delivery interval after membrane rupture.
        J Matern Fetal Neonatal Med. 2017; 30: 772-778