American Journal of Obstetrics and Gynecology (2004) 191, 298e303

www.elsevier.com/locate/ajog

Can shortened midtrimester cervical length predict veryearly spontaneous preterm birth?

John Owen, MD,a Nicole Yost, MD,b Vincenzo Berghella, MD,c

Cora MacPherson, PhD,d Melissa Swain, RN,e Gary A. Dildy III, MD,f

Menachem Miodovnik, MD,g Oded Langer, MD,h Baha Sibai, MD,i

for the Maternal-Fetal Medicine Units Network, Bethesda, Md

University of Alabama at Birminghama; University of Texas Southwestern Medical Center, Dallasb;Thomas Jefferson University, Philadelphia, Pac; George Washington University Biostatistics Center,Bethesda, Md d; Wake Forest University, Winston-Salem, NCe; University of Utah, Salt Lake Cityf;University of Cincinnatig; University of Texas at San Antonioh; University of Tennessee, Memphisi

Received for publication July 18, 2003; revised November 11, 2003; accepted November 18, 2003

––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––Objective: The study was undertaken to test the hypothesis that shortened midtrimester cervical

length is more predictive of early (!26 weeks) than later (26-34 weeks) spontaneous pretermbirth.Study design: This is a secondary analysis of a blinded, multicenter observational study of 183women with a prior preterm birth. Vaginal sonography was begun at 16 to18 weeks’ gestation

and scheduled every 2 weeks (maximum 4 scans per patient). Cervical length and any observeddynamic shortening were recorded at each visit to determine the shortest observed cervical lengthfrom 16 to 24 weeks’ gestation. The shortest cervical length measurements were categorized as less

than 25 mm, 25 to 29 mm and 30 mm or greater. The initial cervical length was also comparedwith the shortest cervical length to categorize patients on the basis of the timing of cervical short-ening 30 mm or less. Contingency table, linear regression, and survival analysis were used to an-

alyze the relationship between cervical length groups and spontaneous preterm birth.Results: In both the less than 25 mm and 25 to 29 mm groups, the incidence of spontaneous mid-trimester birth (!26 weeks) was higher than the incidence of later (26-34 weeks) preterm birth(!25 mm group: 37% vs 19%; 25-29 mm group: 16% vs 3%, respectively) as compared with

women with a shortest cervical length 30 mm or greater, who had rates of 1% and 9% respec-tively (P!.0001). Similarly, women who had an initial cervical length 30 mm or less and thosewho shortened their cervix to 30 mm or less before 22 weeks were also more likely to experience

a midtrimester than later preterm birth, whereas women who shortened their cervix 30 mm or less

KEY WORDSCervical lengthVaginal sonography

Preterm birthMidtrimester birth

Presented at the 2002 Annual Meeting of the Society for Gynecologic Investigation in Los Angeles, Calif, March 21, 2002.

Supported by the following grants from the National Institute of Child Health And Human Development: HD27869, HD21414, HD27860,

HD27905, HD36801, HD34116, HD34210, HD34208, HD34136

Reprints not available from the authors.

E-mail: johnowen@uab.edu

0002-9378/$ - see front matter � 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.ajog.2003.11.025

Owen et al 299

later (22-24 weeks) or who maintained a cervical length greater than 30 mm had lower rates ofmidtrimester than later preterm birth (P!.0001).

Conclusion: Shortened cervical length in the midtrimester preferentially predicts early, as opposedto later, spontaneous preterm birth in high-risk women.� 2004 Elsevier Inc. All rights reserved.

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Preterm birth remains the most significant and chal-lenging problem in obstetrics, owing both to its increas-ing prevalence and associated short-term and permanentneonatal morbidities. Because most cases of pretermbirth can be broadly categorized as spontaneous, andnot the result of maternal/fetal indications,1 contempo-rary research has focused on the identification of womenat risk for spontaneous preterm birth that might benefitfrom appropriate intervention strategies. Although themajority of preterm births in the general population oc-cur near term,2 most of the morbidity and mortality as-sociated with prematurity accrues from delivery before30 weeks’ gestation.

Shortened cervical length in both unselected3,4 andhigh-risk populations5-7 has been shown to be a signifi-cant predictor of spontaneous preterm birth. Cervicallength has also been suggested as a surrogate markerof a continuum of cervical competence,8 which chal-lenges the traditional concept that the cervix is eithercompetent or incompetent. Spontaneous preterm birthhas even been considered a risk factor for cervical in-competence.9

If cervical length is indeed a surrogate for the compe-tency status of the cervix, then women with a shortenedcervical length should be more likely to experience anearly rather than later spontaneous preterm birth. Totest this hypothesis we examined the frequency distribu-tion of spontaneous preterm births in a population ofwomen with prior spontaneous preterm birth that un-derwent serial vaginal sonographic evaluations and cer-vical length assessments in the midtrimester.

Material and methods

This is a secondary analysis of a previously publishedblinded, multicenter, observational study that was ap-proved by the institutional review boards at each ofthe participating centers.5 A total of 183 consentingwomen at high risk for recurrent spontaneous pretermbirth, based on a history of at least 1 prior spontaneouspreterm birth at less than 32 weeks’ gestation, comprisedthe study population. None of these women receiveda prophylactic cerclage because of a clinical history ofcervical incompetence. Vaginal sonography was begunat 16 to 18 weeks’ gestation and scheduled every 2weeks, ending by 24 weeks’ gestation. Sonographers

and sonologists, certified for the study, performed a totalof 590 scans (median 3 scans per patient), and cervicallength was measured from the external os to the internalos along a closed endocervical canal. If a funnel was rec-ognized at the internal os, the length was measured tothe functional internal os, where the apex of the funnelmet the closed endocervical canal. At each vaginal scan,fundal pressure was also applied as a provocative ma-neuver. If fundal pressure-induced or spontaneously oc-curring cervical length shortening was observed, thecervical length was measured again, and the shortest ob-served cervical length for each scan recorded.

By protocol, the results of each scan were not madeavailable to the managing physicians, except in casesof fetal death or complete placenta previa. Sonologistswere also instructed to not inquire about patients’ symp-toms, but were asked to have patients report symptomsto their caregivers; these were not included in the study’sdata acquisition. Similarly, concurrent manual vaginalexaminations were not performed at each sonogram.However, these could be performed by the patient’scaregiver if clinically indicated; these data were alsonot recorded for the observational study. The deliverygestational age and the type of preterm birth (indicatedvs spontaneous) were recorded on all study patients.Spontaneous preterm birth at less than 35 weeks’ gesta-tion was the primary study outcome and was catego-rized on the data forms as primarily the result ofeither preterm rupture of membranes or labor.

For contingency table analysis, we categorized theshortest observed cervical lengths into 3 groups: lessthan 25 mm, 25 to 29 mm, and 30 mm or greater. Wefurther analyzed the relationship between cervical lengthand gestational age at delivery by considering both theinitial cervical length at the first evaluation and any sub-sequent observed shortening. For this we arbitrarily de-fined 4 groups: group 1 included women whose initialcervical length was shortened 30 mm or less, group 2 pa-tients had an initial cervical length greater than 30 mm,but it shortened to 30 mm or less by less than 22 weeks’gestation, group 3 patients also had an initial cervicallength greater than 30 mm, but it shortened to 30 mmor less at or beyond 22 weeks’ gestation. Group 4comprised women who had never had an observed cer-vical length 30 mm or less. We defined midtrimesterbirth as delivery less than 26 weeks and later pretermbirth as delivery at 27 to 34 weeks’ gestation.

300 Owen et al

Continuous data were expressed either as a median ora meanG 1 SD. The c2 test or Fisher exact test was usedto compare categorical data among groups. Linear re-gression was used to model the relationship between theshortest observed cervical length and the scan-to-deliv-ery interval, and survival analysis was used to comparethe scan-to-delivery interval among cervical lengthgroups. Data were analyzed with SAS version 8.0(SAS Institute, Cary, NC) and P!.05 was chosen torepresent statistical significance.

Results

The incidence of spontaneous preterm birth less than 35weeks in the study population was 26%; 3 women whounderwent an indicated preterm birth less than 35weeks’ gestation were included in the group of patientswho were delivered at or beyond 35 weeks. The gesta-tional age at delivery of the study population was35.2G 6.3 weeks. Spontaneous midtrimester birth lessthan 26 weeks complicated 15% (n=28) of pregnan-cies, whereas spontaneous birth at 26 to 34 weeks oc-curred in 11% (n=20). Of the 48 spontaneous pretermbirths less than 35 weeks’ gestation, 14 (29%) occurredafter preterm rupture of membranes, whereas 34(71%) were the result of preterm labor. The proportionsof preterm birth antecedents (membrane rupture or la-bor) were similar across the delivery gestational agegroups (data not shown).

At the initial evaluation at 16 to 18 weeks’ gestation,the median cervical length was 37 mm (interdecile range26-62). The shortest cervical length had a median valueof 30 mm (interdecile range 11-40) and was observed ata median gestational age of 20.9 weeks (range 16-25weeks).

Figure 1 Rates of early (!26 weeks) spontaneous pretermbirth, later (26-34 weeks) spontaneous preterm birth and birth

R35 weeks’ gestation (or indicated preterm birth !35 weeks)in women with prior spontaneous preterm birth !32 weeks’gestation by shortest observed cervical length group

(P!.0001).

The relationship between the shortest observed cervi-

cal length and spontaneous preterm birth is depicted inFigure 1. In both the less than 25 mm and 26 to 29 mmgroups, the incidence of spontaneous midtrimester birth(!26 weeks) was higher than the incidence of later (26-34weeks) preterm birth (!25 mm group: 37% vs 19%; 25-29 mm group: 16% vs 3%, respectively) as comparedwith women with a shortest cervical length 30 mm orgreater, who had rates of 1% and 9% respectively (c2

P!.0001). Only in the latter cervical length group didthe prevalence of spontaneous preterm birth demonstratethe anticipated increase with advancing gestation. Re-sults of the linear regression model are depicted in Figure2. There was a significant linear correlation between theshortest observed cervical length and the latency fromthe sonogram to delivery (P!.0001, r2=0.38).

Figure 3 depicts the relationship between the 4 cervi-cal length groups (which considered both the initial cer-vical length and timing of subsequent cervical lengthshortening) and spontaneous preterm birth. Womenwho had an initial cervical length 30 mm or less (group1) or who shortened their cervixes to 30 mm or less be-fore 22 weeks’ gestation (group 2) were significantlymore likely to experience a spontaneous midtrimesterbirth than women in groups 3 and 4 (P!.0001). Unlikegroups 1 and 2, both women with later cervical shorten-ing (group 3) and women who maintained cervicallengths greater than 30 mm (group 4), demonstrated anincreasing prevalence of spontaneous preterm birth withadvancing gestation. Unlike groups 1 and 2, both womenwith later cervical shortening (group 3) and women whomaintained cervical lengths greater than 30 mm (group4), demonstrated an increasing prevalence of spontane-ous preterm birth with advancing gestation.

Of the 46 women in group 1, 15 (33%) experienceda spontaneous midtrimester birth, whereas 5 (11%) ex-perienced a later spontaneous preterm birth at 26 to34 weeks’ gestation. Of the 21 patients in group 2, 9

Figure 2 Linear regression of shortest observed cervical

length and the scan-to-delivery interval in women with priorspontaneous preterm birth !32 weeks, who underwent serialvaginal sonographic evaluations in the midtrimester.

Owen et al 301

(43%) experienced a midtrimester birth versus 1 (5%)who experienced a later preterm birth. Of 28 in group3, 3 women (11%) experienced a midtrimester birth,and 6 (21%) had a later preterm birth. Finally, of the88 women in group 4, only 1 (1%) experienced a mid-trimester birth versus 8 (9%) who had a later pretermbirth. Of the 20 women in group 1 who experienceda spontaneous preterm birth less than 35 weeks, 70%were coded as antecedent preterm labor versus 60% ofthe 10 preterm births in group 2, 67% of the 9 in group3, and 89% of the 9 observed in group 4 (P=.6 Fisherexact test).

Figure 4 depicts the results of the life-table analysis ofthe 4 cervical length groups with regard to the latencyfrom sonogram to delivery. Shortened cervical lengthidentified at the initial evaluation or which occurred laterin gestation was associated with significantly shorter la-tencies (P!.0001), and women with early shortening atless than 22 weeks had the shortest observed latency. Ap-proximately 40% of women in each of groups 1 and 2experienced a latency period of 4 weeks or less.

Comment

Contemporary models of the spontaneous pretermbirth syndrome acknowledge several key components,including uterine contractions, premature membranerupture, and diminished cervical competence.10 How-ever, it is unknown whether diminished cervical compe-tence is the result of intrinsic mechanical weakness orextrinsic stimuli, as either could lead to prematurecervical ripening and the observation of shortened cer-vical length. If extrinsic processes predominate, thepathophysiologic stimuli (eg, infectious, inflammatory,

Figure 3 Rates of spontaneous preterm birth !26 weeks’, 26to 34 weeks’, and R35 weeks’ gestation (or indicated pretermbirth !35 weeks) in women with prior spontaneous preterm

birth!32 weeks, by initial cervical length%30 mm, the occur-rence of early (!22 week) versus later (R22 week) cervicallength shortening and no observed cervical shortening %30

mm (P!.0001).

hormonal factors) are, in most cases, neither clinicallyapparent nor predictable. Interactions with other ana-tomic components of the preterm birth syndrome mighthasten the preterm birth process and further obscurethe initiating event.

Previous studies3-7 have confirmed an inverse rela-tionship between cervical length, as measured with vag-inal sonography, and the risk of preterm birth.Nevertheless, the relationship between shortened cervi-cal length in the midtrimester and the timing of sub-sequent spontaneous preterm birth has not been wellcharacterized in high-risk women. Andrews et al,6 ina blinded, cross-sectional study of high-risk women,noted that those with a shortened cervical length weremore likely to deliver within 4 weeks of their evaluationthan women with longer cervical lengths, but they didnot compare the frequencies of early versus later sponta-neous preterm birth. Heath et al,4 in a study of 2567 un-selected gravid women, observed the typical inverserelationship between cervical length and the risk of pre-term birth, and used receiver operator characteristics tosuggest that cervical length might be a better predictorof early (!28 weeks) versus later preterm birth. In a re-port of 469 women with various anatomic and historicrisk factors for preterm birth, Guzman et al11 performedlongitudinal evaluations of the cervix with vaginal so-nography. However, the results were used for both pa-tient management and for scheduling follow-upsonograms. Guzman et al11 also used receiver operatorcharacteristics and concluded that cervical length wasthe best predictor of preterm birth and that it was morestrongly associated with early (!30 weeks) than later(!34 weeks) preterm birth.

Shortened midtrimester cervical length has alsobeen investigated as a diagnostic criterion for cervical

Figure 4 Survival analysis depicting undelivered rates inwomen with prior spontaneous preterm birth !32 weeks,according to whether: A, the initial cervical length was %30

mm; B, there was observed cervical length shortening%30 mmat !22 weeks; C, there was observed cervical lengthshortening %30 mm at R22 weeks; or D, the cervical lengthremainedO30 mm during serial evaluations (P!.0001).

302 Owen et al

incompetence,12-14 although the results of both retro-spective cohort series15-17 and randomized trials18,19 ofcerclage in women with a shortened midtrimester cervicallength have been conflicting and inconclusive. Explana-tions for these inconsistent results, and our observationthat many women with shortened cervical length in themidtrimester do not ultimately experience a pretermbirth, include the possibility that, because of biologicvariation, some women simply have a shortened cervicallength, but otherwise normal cervical function, and noconcurrent pathophysiologic stimuli for preterm birth.In other cases, pathophysiologic stimuli may have com-menced, leading to some cervical shortening, but the pro-cess abates, either spontaneously or because of intrinsiclocal or systemic defensemechanisms. Lastly, a shortenedcervical length could represent an example of covert me-chanical weakness, insufficient to reach a clinically sig-nificant threshold in any particular gestation.

One limitation to our study is that specific detaileddelivery information was not collected, and so we wereunable to determine, even in retrospect, how manywomen presented with characteristic symptoms andphysical findings suggesting a clinical diagnosis of cervi-cal incompetence: preterm births were only character-ized as primarily the result of labor or membranerupture. Nevertheless, because of possible interactionsamong components of the preterm birth syndrome, itis plausible that some patients, as a result of diminishedcervical competence, developed concurrent pathophysi-ologic stimuli that ultimately led to clinical manifesta-tions of membrane rupture or labor.20

Collectively, the results of our study and others4,11

suggest that at least a portion of high-risk women withshortened midtrimester cervical length may have a clini-cally significant element of diminished cervical compe-tence, because shortened midtrimester cervical length ispreferentially associated with midtrimester versus later-occurring spontaneous preterm birth. In particular,women who have a shortened cervical length early inthe midtrimester or who shorten their cervix to 30 mmor less before 22 weeks’ gestation are at particularly highrisk to experience a spontaneous midtrimester birth.Randomized intervention trials of preventive strategiesin women with a prior spontaneous preterm birth andshortened midtrimester cervical length, and investiga-tions into the specific stimuli and mechanisms associatedwith individualized pathways to prematurity are needed.

Acknowledgments

We acknowledge the other members of the Maternal-Fetal Medicine Units Network and their contributionsas follows: University of Alabama at Birmingham:Cherry Neely, RT, RDMS (study design, sonologist cer-tification and sonography); Allison Northen, RN (data

collection); John C. Hauth, MD (study design); DebbieThom, RT, RDMS (sonography); University of Chica-go: Atef H. Moawad, MD (study design); Universityof Cincinnati: Nancy Elder, MSN, RN (data collection);Tammy Haskins (sonography); Deni Schultz (sonogra-phy); George Washington University Biostatistics Cen-ter: Elizabeth Thom, PhD (study design, data analysisand data quality assurance); Sharon Leindecker, MS(data quality assurance); Magee Women’s Hospital:Steve N. Caritis, MD (study design); University of Mi-ami: Mary Jo O’Sullivan, MD (study design); NationalInstitute of Child Health and Human Development:Charlotte Catz, MD (funding); Sumner J. Yaffe, MD(funding); Cathy Spong, MD (manuscript editing); OhioState University: Jay D. Iams, MD (study design andmanuscript editing); University of Tennessee: RisaRamsey, BSN, RN (data collection); Mary Peterson (so-nography); Joyce Fricke (sonography); Jeff Livingston(sonography); University of Texas at San Antonio: Sus-an Barker, RN (data collection); Connie Leija (sonogra-phy); University of Texas, Southwestern: Kenneth J.Leveno, MD (study design and manuscript editing); Ju-lia McCampbell, BSN, RN (data collection); RebeccaBenezue (sonography); Thomas Jefferson University:Michelle DiVito, RN, MSN (data collection); RonaldJ. Wapner, MD (study design); George Bega (sonogra-phy); University of Utah: Micheal W. Varner, MD(study design); Elaine Taggart, RN (data collection);Ruth Zollinger (sonography); Wake Forest University:Paul Meis, MD (study design), Allison Henshaw (sonog-raphy); Wayne State University: Mitchell Dombrowski,MD (study design).

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