Advertisement

Precocious cervical ripening as a screening target to predict spontaneous preterm delivery among asymptomatic singleton pregnancies: a systematic review

      Routine second-trimester transvaginal ultrasonographic (TVU) screening for short cervical length (CL) predicts spontaneous preterm delivery (SPTD), albeit with limited sensitivity (35-40%) and a moderate positive likelihood ratio of 4-6. However, CL describes one of the multidimensional changes that are associated with precocious cervical ripening (PCCR) and that also include cervical softening, cervical funneling (CF), and dilation. PCCR, a precursor and a strong predictor for SPTD, was proposed as a potential screening target. We hypothesized that screening for composite measures of PCCR (eg, CL, CF, cervical consistency, and dilation) with the use of either digital examination or TVU would improve the prediction of SPTD compared with screening for short CL alone. We searched PubMed and EMBASE electronic databases for observational cohort studies to evaluate cervical screening in asymptomatic obstetric populations. Multidimensional composite cervical measures were assessed in 10 datasets (n = 22,050 pregnancies) and 12 publications. Appreciable heterogeneity in cervical measurements, data quality, and outcomes across studies prevented quantitative metaanalysis. Only one study reported intra- and interobserver reliability of cervical measurements. The prevalence of CF ranged from 0.7–9.1%. Five studies compared composite measures of PCCR (ie, CL and CF) with short CL alone and consistently reported improved screening performance. Among 3 TVU studies, gains in sensitivity ranged from 5–27%, and increases in positive likelihood ratio ranged from 3–16. Our findings suggest that composite measures of PCCR might serve as valuable screening targets. High-quality interdisciplinary studies that integrate epidemiologic approaches are needed to test this hypothesis and to accelerate the translation of advances in cervical pathophysiology into effective preventive interventions.

      Key words

      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 American Journal of Obstetrics & Gynecology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Holzman C.
        • Paneth N.
        Preterm birth: from prediction to prevention.
        Am J Public Health. 1998; 88: 183-184
        • Iams J.D.
        • Romero R.
        • Culhane J.F.
        • Goldenberg R.L.
        Primary, secondary, and tertiary interventions to reduce the morbidity and mortality of preterm birth.
        Lancet. 2008; 371: 164-175
        • March of Dimes; the Partnership for Maternal Newborn and Child Health; Save the Children; World Health Organization
        Born too soon: the global action report on preterm birth.
        in: Howson C. Kinney M. Lawn J.E. World Health Organization, Geneva2012 (Available at:) (Accessed Sept. 7, 2012)
        • Holland W.W.
        • Stewart S.
        Screening in disease prevention: what works?.
        Radcliffe Publishing Ltd, Oxford2005
        • Harris R.
        • Sawaya G.F.
        • Moyer V.A.
        • Calonge N.
        Reconsidering the criteria for evaluating proposed screening programs: reflections from 4 current and former members of the U.S. Preventive services task force.
        Epidemiol Rev. 2011; 33: 20-35
        • Owen J.
        • Iams J.D.
        • National Institute of Child H, Human Development Maternal-Fetal Medicine Units N
        What we have learned about cervical ultrasound.
        Semin Perinatol. 2003; 27: 194-203
        • ACOG Committee on Practice Bulletins
        Prediction and prevention of preterm birth. ACOG Practice bulletin no. 130.
        Obstet Gynecol. 2012; 120: 964-973
        • Iams J.D.
        • Goldenberg R.L.
        • Meis P.J.
        • et al.
        The length of the cervix and the risk of spontaneous premature delivery: National Institute of Child Health and Human Development Maternal Fetal Medicine Unit Network.
        N Engl J Med. 1996; 334: 567-572
        • Honest H.
        • Bachmann L.M.
        • Coomarasamy A.
        • Gupta J.K.
        • Kleijnen J.
        • Khan K.S.
        Accuracy of cervical transvaginal sonography in predicting preterm birth: a systematic review.
        Ultrasound Obstet Gynecol. 2003; 22: 305-322
        • Crane J.M.
        • Hutchens D.
        Transvaginal sonographic measurement of cervical length to predict preterm birth in asymptomatic women at increased risk: a systematic review.
        Ultrasound Obstet Gynecol. 2008; 31: 579-587
        • Honest H.
        • Forbes C.A.
        • Duree K.H.
        • et al.
        Screening to prevent spontaneous preterm birth: systematic reviews of accuracy and effectiveness literature with economic modelling.
        Health Technol Assess. 2009; 13: 1-627
        • Honest H.
        • Hyde C.J.
        • Khan K.S.
        Prediction of spontaneous preterm birth: no good test for predicting a spontaneous preterm birth.
        Curr Opin Obstet Gynecol. 2012; 24: 422-433
        • Romero R.
        • Nicolaides K.
        • Conde-Agudelo A.
        • et al.
        Vaginal progesterone in women with an asymptomatic sonographic short cervix in the midtrimester decreases preterm delivery and neonatal morbidity: a systematic review and metaanalysis of individual patient data.
        Am J Obstet Gynecol. 2012; 206: 124.e1-124.e19
        • Cahill A.G.
        • Odibo A.O.
        • Caughey A.B.
        • et al.
        Universal cervical length screening and treatment with vaginal progesterone to prevent preterm birth: a decision and economic analysis.
        Am J Obstet Gynecol. 2010; 202: 548.e1-548.e8
        • Werner E.F.
        • Han C.S.
        • Pettker C.M.
        • et al.
        Universal cervical-length screening to prevent preterm birth: a cost-effectiveness analysis.
        Ultrasound Obstet Gynecol. 2011; 38: 32-37
        • Odibo A.O.
        • Stamilio D.M.
        • Macones G.A.
        • Polsky D.
        17alpha-hydroxyprogesterone caproate for the prevention of preterm delivery: a cost-effectiveness analysis.
        Obstet Gynecol. 2006; 108: 492-499
        • Parry S.
        • Simhan H.
        • Elovitz M.
        • Iams J.
        Universal maternal cervical length screening during the second trimester: pros and cons of a strategy to identify women at risk of spontaneous preterm delivery.
        Am J Obstet Gynecol. 2012; 207: 101-106
        • American College of Obstetricians Gynecologists
        Ultrasonography in pregnancy. ACOG Practice bulletin no. 101.
        Obstet Gynecol. 2009; 113: 451-461
      1. US Preventive Services Task Force. Screening for bacterial vaginosis in pregnancy to prevent preterm delivery: The US Preventive Services Task Force, February 2008. Available at: http://www.uspreventiveservicestaskforce.org/uspstf/uspsbvag.htm#clinical. Accessed Dec. 19, 2012.

      2. US Preventive Services Task Force. Screening for ultrasonography in pregnancy: The US Preventive Services Task Force, 1996. Available at: http://www.uspreventiveservicestaskforce.org/uspstf/uspsuspg.htm. Accessed Jan. 1, 2013.

        • US Preventive Services Task Force
        Screening for bacterial vaginosis in pregnancy to prevent preterm delivery: US Preventive Services Task Force recommendation statement.
        Ann Intern Med. 2008; 148: 214-219
        • Bishop E.
        Pelvic scoring for elective induction.
        Obstet Gynecol. 1964; 24: 266-268
        • Wood C.
        • Bannerman R.H.
        • Booth R.T.
        • Pinkerton J.H.
        The prediction of premature labor by observation of the cervix and external tocography.
        Am J Obstet Gynecol. 1965; 91: 396-402
      3. Papiernik E, Keith L, Bouyer J, Dreyfus J, Lazar P. Effective prevention of preterm birth: the French experience measured at Haguenau. White Plains, NY: March of Dimes Birth Defects Foundation; 1989.

        • Papiernik E.
        • Bouyer J.
        • Dreyfus J.
        • et al.
        Prevention of preterm births: a perinatal study in Haguenau, France.
        Pediatrics. 1985; 76: 154-158
        • Papiernik E.
        • Kaminski M.
        Multifactorial study of the risk of prematurity at 32 weeks of gestation: I, a study of the frequency of 30 predictive characteristics.
        J Perinat Med. 1974; 2: 30-36
        • Papiernik E.
        • Bouyer J.
        • Collin D.
        • Winisdoerffer G.
        • Dreyfus J.
        Precocious cervical ripening and preterm labor.
        Obstet Gynecol. 1986; 67: 238-242
        • Papiernik E.
        • Spira N.
        • Bréart G.
        [prévention de la naissnace prématurée: nouveaux objectifs et nouvelles pratiques des soins prénataux (prevention of preterm birth: new goals and new practices in prenatal care): colloque INSERM, Evian, 19–22 mai 1985].
        INSERM, Paris, France1986
        • Papiernik E.
        • Charlemain C.
        • Goffinet F.
        • Paul G.
        • Keith L.
        Vaginal bacterial colonization, uterine cervix and preterm births.
        PrenatNeonat Med. 1998; 3: 98-102
        • Alexander G.R.
        • Weiss J.
        • Hulsey T.C.
        • Papiernik E.
        Preterm birth prevention: an evaluation of programs in the United States.
        Birth. 1991; 18: 160-169
        • Wald N.
        • Law M.
        Medical screening.
        in: Warrell D.A. Cox T.M. Firth J.D. Oxford textbook of medicine, vol. 1. 5th ed. Oxford University Press, New York2010: 94-108
        • Wacholder S.
        Precursors in cancer epidemiology: aligning definition and function.
        Cancer Epidemiol Biomarkers Prev. 2013; 22: 521-527
        • Challis J.R.G.
        Mechanism of parturition and preterm labor.
        Obstet Gynecol Surv. 2000; 55: 650-660
      4. Institute of Medicine Committee on Understanding Premature Birth Assuring Healthy Outcomes. Preterm birth: causes, consequences, and prevention. Washington, DC: National Academy of Sciences; 2007.

      5. Morrison AS. Screening. In: Rothman KJ, Greenland S, eds. Modern epidemiology. Philadelphia: Lippincott-Raven Publishers; 1998:499-518.

        • Berghella V.
        • Bega G.
        Ultrasound evaluation of the cervix.
        in: Callen P.W. Ultrasonography in obstetrics and gynecology. Saunders Elsevier, Philadelphia2008: 698-720
        • Zilianti M.
        • Azuaga A.
        • Calderon F.
        • Pages G.
        • Mendoza G.
        Monitoring the effacement of the uterine cervix by transperineal sonography: a new perspective.
        J Ultrasound Med. 1995; 14: 719-724
        • Word R.A.
        • Li X.H.
        • Hnat M.
        • Carrick K.
        Dynamics of cervical remodeling during pregnancy and parturition: mechanisms and current concepts.
        Semin Reprod Med. 2007; 25: 69-79
        • Word R.A.
        • Li X.-H.
        Cervical function during pregnancy and parturition.
        in: Petraglia F. Strauss J. Gabbe S.G. Weiss G. Preterm birth: mechanisms, mediators, prediction & interventions. Taylor & Francis Medical Books, Abingdon OX, UK2006: 19-34
        • Darios E.S.
        • Seitz B.
        • Watts S.W.
        Smooth muscle pharmacology in the isolated virgin and pregnant rat uterus and cervix.
        J Pharmacol Exp Ther. 2012; 341: 587-596
        • Romero R.
        • Espinoza J.
        • Kusanovic J.P.
        • et al.
        The preterm parturition syndrome.
        BJOG. 2006; 113: 17-42
        • Romero R.
        • Mazor M.
        • Munoz H.
        • Gomez R.
        • Galasso M.
        • Sherer D.M.
        The preterm labor syndrome.
        Ann N Y Acad Sci. 1994; 734: 414-429
        • Goldenberg R.L.
        • Gravett M.G.
        • Iams J.
        • et al.
        The preterm birth syndrome: issues to consider in creating a classification system.
        Am J Obstet Gynecol. 2012; 206: 113-118
        • Caritis S.N.
        • Simhan H.
        Cervical pessary use and preterm birth: how little we know.
        Lancet. 2012; 379: 1769-1770
        • Owen J.
        • Iams J.D.
        • Hauth J.C.
        Vaginal sonography and cervical incompetence.
        Am J Obstet Gynecol. 2003; 188: 586-596
        • Iams J.D.
        • Johnson F.F.
        • Sonek J.
        • Sachs L.
        • Gebauer C.
        • Samuels P.
        Cervical competence as a continuum: a study of ultrasonographic cervical length and obstetric performance.
        Am J Obstet Gynecol. 1995; 172: 1097-1106
        • Harger J.H.
        Cerclage and cervical insufficiency: an evidence-based analysis.
        Obstet Gynecol. 2002; 100: 1313-1327
        • Reiter E.
        • Nielsen K.A.
        • Fedder J.
        Digital examination and transvaginal scan: competing or complementary for predicting preterm birth?.
        Acta Obstet Gynecol Scand. 2012; 91: 428-438
        • Berghella V.
        • Baxter J.K.
        • Hendrix N.W.
        Cervical assessment by ultrasound for preventing preterm delivery.
        Cochrane Database Syst Rev. 2013; : CD007235
        • Lim A.C.
        • Hegeman M.A.
        • Huis In ‘T Veld M.A.
        • Opmeer B.C.
        • Bruinse H.W.
        • Mol B.W.
        Cervical length measurement for the prediction of preterm birth in multiple pregnancies: a systematic review and bivariate meta-analysis.
        Ultrasound Obstet Gynecol. 2011; 38: 10-17
        • Berghella V.
        Universal cervical length screening for prediction and prevention of preterm birth.
        Obstet Gynecol Surv. 2012; 67: 653-658
        • Leitich H.
        • Brunbauer M.
        • Kaider A.
        • Egarter C.
        • Husslein P.
        Cervical length and dilatation of the internal cervical os detected by vaginal ultrasonography as markers for preterm delivery: a systematic review.
        Am J Obstet Gynecol. 1999; 181: 1465-1472
        • Barros-Silva J.
        • Pedrosa A.C.
        • Matias A.
        Sonographic measurement of cervical length as a predictor of preterm delivery: a systematic review.
        J Perinat Med. 2013; : 1-13
        • Adriaensen W.J.
        • Mathei C.
        • Buntinx F.J.
        • Arbyn M.
        A framework provided an outline toward the proper evaluation of potential screening strategies.
        J Clin Epidemiol. 2013; 66: 639-647
        • Timor-Tritsch I.E.
        • Boozarjomehri F.
        • Masakowski Y.
        • Monteagudo A.
        • Chao C.R.
        Can a “snapshot” sagittal view of the cervix by transvaginal ultrasonography predict active preterm labor?.
        Am J Obstet Gynecol. 1996; 174: 990-995
        • Heath V.C.
        • Southall T.R.
        • Souka A.P.
        • Elisseou A.
        • Nicolaides K.H.
        Cervical length at 23 weeks of gestation: prediction of spontaneous preterm delivery.
        Ultrasound Obstet Gynecol. 1998; 12: 312-317
        • To M.S.
        • Skentou C.A.
        • Royston P.
        • Yu C.K.
        • Nicolaides K.H.
        Prediction of patient-specific risk of early preterm delivery using maternal history and sonographic measurement of cervical length: a population-based prospective study.
        Ultrasound Obstet Gynecol. 2006; 27: 362-367
        • Hassan S.S.
        • Romero R.
        • Berry S.M.
        • et al.
        Patients with an ultrasonographic cervical length ≤15 mm have nearly a 50% risk of early spontaneous preterm delivery.
        Am J Obstet Gynecol. 2000; 182: 1458-1467
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        • PRISMA Group
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        J Clin Epidemiol. 2009; 62: 1006-1012
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        • PRISMA Group
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        Ann Intern Med. 2009; 151 (W64): 264-269
        • Bouyer J.
        • Papiernik E.
        • Dreyfus J.
        • Collin D.
        • Winisdoerffer B.
        • Gueguen S.
        Maturation signs of the cervix and prediction of preterm birth.
        Obstet Gynecol. 1986; 68: 209-214
        • Leung T.N.
        • Pang M.W.
        • Leung T.Y.
        • Poon C.F.
        • Wong S.M.
        • Lau T.K.
        Cervical length at 18-22 weeks of gestation for prediction of spontaneous preterm delivery in Hong Kong Chinese women.
        Ultrasound Obstet Gynecol. 2005; 26: 713-717
        • Taipale P.
        • Hiilesmaa V.
        Sonographic measurement of uterine cervix at 18-22 weeks’ gestation and the risk of preterm delivery.
        Obstet Gynecol. 1998; 92: 902-907
        • To M.S.
        • Skentou C.
        • Liao A.W.
        • Cacho A.
        • Nicolaides K.H.
        Cervical length and funneling at 23 weeks of gestation in the prediction of spontaneous early preterm delivery.
        Ultrasound Obstet Gynecol. 2001; 18: 200-203
        • Mortensen O.A.
        • Franklin J.
        • Lofstrand T.
        • Svanberg B.
        Prediction of preterm birth.
        Acta Obstet Gynecol Scand. 1987; 66: 507-512
        • Fletcher R.
        • Fletcher S.W.
        • Fletcher G.S.
        Diagnosis.
        in: Fletcher R. Fletcher S.W. Fletcher G.S. Clinical epidemiology: the essentials. 5th ed. Lippincott Williams & Wilkins, Philadelphia2013: 93-107
        • Pires C.R.
        • Moron A.F.
        • Mattar R.
        • Diniz A.L.
        • Andrade S.G.
        • Bussamra L.C.
        Cervical gland area as an ultrasonographic marker for preterm delivery.
        Int J Gynaecol Obstet. 2006; 93: 214-219
        • Owen J.
        • Neely C.
        • Northen A.
        Transperineal versus endovaginal ultrasonographic examination of the cervix in the midtrimester: a blinded comparison.
        Am J Obstet Gynecol. 1999; 181: 780-783
        • Roh H.J.
        • Ji Y.I.
        • Jung C.H.
        • Jeon G.H.
        • Chun S.
        • Cho H.J.
        Comparison of cervical lengths using transabdominal and transvaginal sonography in midpregnancy.
        J Ultrasound Med. 2013; 32: 1721-1728
        • Mara M.
        • Calda P.
        • Haakova L.
        • Zizka Z.
        • Dohnalova A.
        • Zivny J.
        Significance of ultrasound vaginal cervicometry in predicting preterm delivery.
        Med Sci Monit. 2002; 8: MT72-MT77
        • Whiting P.
        • Rutjes A.W.
        • Reitsma J.B.
        • Bossuyt P.M.
        • Kleijnen J.
        The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews.
        BMC Med Res Methodol. 2003; 3: 25
        • Bossuyt P.M.
        • Reitsma J.B.
        • Bruns D.E.
        • et al.
        Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative.
        BMJ. 2003; 326: 41-44
        • Deeks J.J.
        Systematic reviews in health care: systematic reviews of evaluations of diagnostic and screening tests.
        BMJ. 2001; 323: 157-162
      6. Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions. West Sussex, England: The Cochrane Collaboration and John Wiley & Sons Ltd; 2008.

        • Hartmann K.
        • Thorp J.M.
        • McDonald T.L.
        • Savitz D.A.
        • Granados J.L.
        Cervical dimensions and risk of preterm birth: a prospective cohort study.
        Obstet Gynecol. 1999; 93: 504-509
        • De Carvalho M.H.
        • Bittar R.E.
        • Brizot Mde L.
        • Bicudo C.
        • Zugaib M.
        Prediction of preterm delivery in the second trimester.
        Obstet Gynecol. 2005; 105: 532-536
        • Newman R.B.
        • Goldenberg R.L.
        • Iams J.D.
        • et al.
        Preterm prediction study: comparison of the cervical score and Bishop score for prediction of spontaneous preterm delivery.
        Obstet Gynecol. 2008; 112: 508-515
        • To M.S.
        • Skentou C.
        • Cicero S.
        • Liao A.W.
        • Nicolaides K.H.
        Cervical length at 23 weeks in triplets: prediction of spontaneous preterm delivery.
        Ultrasound Obstet Gynecol. 2000; 16: 515-518
        • Mercer B.M.
        • Goldenberg R.L.
        • Das A.
        • et al.
        The preterm prediction study: a clinical risk assessment system.
        Am J Obstet Gynecol. 1996; 174: 1885-1895
        • Parra-Saavedra M.
        • Gomez L.
        • Barrero A.
        • Parra G.
        • Vergara F.
        • Navarro E.
        Prediction of preterm birth using the cervical consistency index.
        Ultrasound Obstet Gynecol. 2011; 38: 44-51
        • Hasegawa I.
        • Tanaka K.
        • Takahashi K.
        • et al.
        Transvaginal ultrasonographic cervical assessment for the prediction of preterm delivery.
        J Matern Fetal Med. 1996; 5: 305-309
        • Houlton M.C.
        • Marivate M.
        • Philpott R.H.
        Factors associated with preterm labour and changes in the cervix before labour in twin pregnancy.
        BJOG. 1982; 89: 190-194
        • Marivate M.
        • De Villiers K.Q.
        • Fairbrother P.
        Effect of prophylactic outpatient administration of fenoterol on the time of onset of spontaneous labor and fetal growth rate in twin pregnancy.
        Am J Obstet Gynecol. 1977; 128: 707-708
        • Neilson J.P.
        • Verkuyl D.A.
        • Crowther C.A.
        • Bannerman C.
        Preterm labor in twin pregnancies: prediction by cervical assessment.
        Obstet Gynecol. 1988; 72: 719-723
        • Blencowe H.
        • Cousens S.
        • Oestergaard M.Z.
        • et al.
        National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications.
        Lancet. 2012; 379: 2162-2172
        • Heath V.C.
        • Southall T.R.
        • Souka A.P.
        • Novakov A.
        • Nicolaides K.H.
        Cervical length at 23 weeks of gestation: relation to demographic characteristics and previous obstetric history.
        Ultrasound Obstet Gynecol. 1998; 12: 304-311
        • Brieger G.M.
        • Xie H.N.
        • Dawkins R.R.
        • et al.
        Transvaginal sonographic assessment of cervical dynamics during the third trimester of normal pregnancy.
        Acta Obstet Gynecol Scand. 1997; 76: 118-122
        • Erasmus I.
        • Nicolaou E.
        • Van Gelderen C.J.
        • Nicolaides K.H.
        Cervical length at 23 weeks’ gestation: relation to demographic characteristics and previous obstetric history in South African women.
        S Afr Med J. 2005; 95: 691-695
        • Feltovich H.
        • Hall T.J.
        Quantitative imaging of the cervix: setting the bar.
        Ultrasound Obstet Gynecol. 2013; 41: 121-128
        • Berghella V.
        • Owen J.
        • Macpherson C.
        • et al.
        Natural history of cervical funneling in women at high risk for spontaneous preterm birth.
        Obstet Gynecol. 2007; 109: 863-869
        • Li Q.
        • Zhang J.
        • You Z.
        [Cervical ripening score by transperineal ultrasonography and its predictive effect for induction of labor by prostaglandin E2].
        Chinese J Obstet Gynecol (in Chinese). 1998; 33: 216-218
        • Reeves M.J.
        • Curtis C.R.
        • Salman M.D.
        • Stashak T.S.
        • Reif J.S.
        Multivariable prediction model for the need for surgery in horses with colic.
        Am J Vet Res. 1991; 52: 1903-1907
        • Pencina M.J.
        • D’Agostino R.B.
        • Pencina K.M.
        • Janssens A.C.
        • Greenland P.
        Interpreting incremental value of markers added to risk prediction models.
        Am J Epidemiol. 2012; 176: 473-481
        • Morrow-Howell N.
        The M word: multicollinearity in multiple regression.
        Social Work Res. 1994; 18: 247-262
        • Salomon L.J.
        • Diaz-Garcia C.
        • Bernard J.P.
        • Ville Y.
        Reference range for cervical length throughout pregnancy: non-parametric LMS-based model applied to a large sample.
        Ultrasound Obstet Gynecol. 2009; 33: 459-464
        • Berghella V.
        • Roman A.
        • Daskalakis C.
        • Ness A.
        • Baxter J.K.
        Gestational age at cervical length measurement and incidence of preterm birth.
        Obstet Gynecol. 2007; 110: 311-317
        • Owen J.
        • Yost N.
        • Berghella V.
        • et al.
        Mid-trimester endovaginal sonography in women at high risk for spontaneous preterm birth.
        JAMA. 2001; 286: 1340-1348
        • Guzman E.R.
        • Walters C.
        • Ananth C.V.
        • et al.
        A comparison of sonographic cervical parameters in predicting spontaneous preterm birth in high-risk singleton gestations.
        Ultrasound Obstet Gynecol. 2001; 18: 204-210
        • Feltovich H.
        • Hall T.J.
        • Berghella V.
        Beyond cervical length: emerging technologies for assessing the pregnant cervix.
        Am J Obstet Gynecol. 2012; 207: 345-354
        • Goldenberg R.L.
        • Iams J.D.
        • Das A.
        • et al.
        The Preterm Prediction Study: sequential cervical length and fetal fibronectin testing for the prediction of spontaneous preterm birth: National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network.
        Am J Obstet Gynecol. 2000; 182: 636-643
        • Espinoza J.
        • Goncalves L.F.
        • Romero R.
        • et al.
        The prevalence and clinical significance of amniotic fluid ‘sludge’ in patients with preterm labor and intact membranes.
        Ultrasound Obstet Gynecol. 2005; 25: 346-352
        • Himaya E.
        • Rhalmi N.
        • Girard M.
        • et al.
        Midtrimester intra-amniotic sludge and the risk of spontaneous preterm birth.
        Am J Perinatol. 2011; 28: 815-820
        • Arabin B.
        • Aardenburg R.
        • Van Eyck J.
        Maternal position and ultrasonic cervical assessment in multiple pregnancy: preliminary observations.
        J Reprod Med. 1997; 42: 719-724
        • Arabin B.
        • Roos C.
        • Kollen B.
        • Van Eyck J.
        Comparison of transvaginal sonography in recumbent and standing maternal positions to predict spontaneous preterm birth in singleton and twin pregnancies.
        Ultrasound Obstet Gynecol. 2006; 27: 377-386
      7. National Institutes of Health. Preterm birth in nulliparous women: an understudied population at great risk (U10), 2008. Available at: http://grants.nih.gov/grants/guide/rfa-files/RFA-HD-08-029.html . Accessed July 20, 2012.

        • Reece E.A.
        A clarion call for translational and collaborative research.
        Am J Obstet Gynecol. 2006; 194: 1507-1509
        • Khoury M.J.
        • Gwinn M.
        • Ioannidis J.P.
        The emergence of translational epidemiology: from scientific discovery to population health impact.
        Am J Epidemiol. 2010; 172: 517-524
        • Hiatt R.A.
        Epidemiology: key to translational, team, and transdisciplinary science.
        Ann Epidemiol. 2008; 18: 859-861
        • Viera A.J.
        Predisease: when does it make sense?.
        Epidemiol Rev. 2011; 33: 122-134