Original Article
Fetal Fibronectin in Cervical and Vaginal Secretions as a Predictor of Preterm Delivery
N Engl J Med 1991; 325:669-674September 5, 1991
- Abstract
- Abstract
Background.
Preterm delivery is the leading cause of neonatal mortality in the United States, but efforts to address the problem are hampered by the inability to predict accurately which pregnancies are at risk. We postulated that damage to the fetal membranes may release fetal fibronectin into the cervix and vagina, giving rise to a biochemical marker for preterm delivery.
Methods.
We measured fetal-fibronectin concentrations in cervical and vaginal secretions, amniotic fluid, and maternal plasma with a sensitive immunoassay using the monoclonal antibody FDC-6. Immunohistochemical studies were used to determine the distribution of fetal fibronectin in the placenta and amniochorionic membranes and to ascertain its cell of origin.
Results.
Women with uncomplicated pregnancies (n = 163) who delivered at term rarely had cervicovaginal fetal-fibronectin concentrations above 0.05 μg per milliliter between 21 and 37 weeks of gestation (11 of 267 cervical samples [4 percent] and 9 of 267 vaginal samples [3 percent]). High levels of fetal fibronectin were detected in amniotic fluid and in the cervical or vaginal secretions of 93.8 percent of the women with preterm rupture of membranes (n = 65). Cervical or vaginal fetal fibronectin was also present in 50.4 percent of the women with preterm uterine contractions and intact membranes (n = 117), and its presence identified the women who delivered before term (n = 60) with a sensitivity of 81.7 percent and a specificity of 82.5 percent. In the placenta and membranes, fetal fibronectin was found at points of contact with the uterine wall.
Conclusions.
The presence of cervicovaginal fetal fibronectin in the second and third trimesters of pregnancy identifies a subgroup of women who are at high risk for preterm delivery. This phenomenon may reflect the separation of the chorion from the decidual layer of the uterus, with the release of intact or degraded chorionic components of the extracellular matrix into the cervical and vaginal secretions. (N Engl J Med 1991; 325:669–74.)
Media in This Article
Figure 1
Percentage of Cervical and Posterior Vaginal Forniceal Samples with Fetal Fibronectin, According to Week of Gestation, in Patients with Uncomplicated Pregnancies Who Delivered at Term.Figure 2
Immunohistochemical Studies of Fetal Fibronectin.Article Activity
- Article
DELIVERY of infants before the completion of 37 weeks of gestation is the leading cause of neonatal morbidity and mortality in the United States.1 Current methods of identifying the women who will deliver before term rely on obstetrical history, demographic factors, or premonitory symptoms that are neither sensitive nor specific.2 Moreover, current treatment regimens are frequently hampered by an advanced stage of labor or the inability to distinguish between irrelevant contractions and true preterm labor.
This obstetrical problem might be solved if an early, objective biochemical marker for preterm delivery were identified. Previous candidates (e.g., plasma estradiol-17β, progesterone, and C-reactive protein) have not withstood rigorous scrutiny. Fibronectins are a family of ubiquitous proteins found in the plasma and extracellular matrix. A unique moiety identified in amniotic fluid, extracts of placental tissue, and malignant cell lines contains an epitope termed the "oncofetal domain" that is recognized by the monoclonal antibody FDC-6.3 4 5 This epitope results from the addition of α-N-acetylgalactosamine to a threonine residue in a hexapeptide segment (Val-Thr-His-Pro-Gly-Tyr) located in the IIICS (connecting segment) variable region of fibronectin. We postulated that since fetal fibronectin is present in amniotic fluid and placental tissue,3 mechanical or inflammatory-mediated damage to the membranes6 , 7 before preterm delivery might result in its release into the cervix and vagina.
We undertook a multicenter study to evaluate pregnant women for the presence of fetal fibronectin in their cervical and vaginal secretions and to relate its presence to the risk of preterm delivery. Concentrations of fetal fibronectin were also measured in amniotic fluid, neonatal urine, and maternal plasma. Immunohistochemical studies were subsequently undertaken to determine the location of fetal fibronectin in the placenta and membranes.
Methods
Clinical Studies
Study Patients
Studies were conducted at three medical centers (St. Margaret's Hospital, Boston; Mount Sinai Medical Center, New York; and the University of California at Irvine). The two study groups were made up of patients evaluated for admission to the hospital for either preterm rupture of membranes (n = 65) or preterm contractions with intact membranes (n = 117) for whom precise gestational dating was available.
Preterm rupture of membranes was defined as rupture of membranes before 37 weeks of gestation, with or without regular uterine contractions. Membrane rupture was defined as the presence of two or more of the following: gross pooling of amniotic fluid, an alkaline vaginal pH on Nitrazine paper, ferning of dried vaginal secretions on microscopy, and ultrasonographic diagnosis of a decreased volume of amniotic fluid.
The group with preterm contractions had increasingly symptomatic uterine contractions before 37 weeks of gestation but did not have more than one criterion of membrane rupture (81 percent had none). In patients without clinical evidence of preterm rupture of membranes, the cervix was assessed for length, effacement, and dilatation. Both the group with preterm rupture of membranes and that with preterm contractions were monitored to assess the frequency of contractions and the pattern of the fetal heart rate. Tocolytic therapy was administered at the discretion of the attending physician and included intravenous magnesium sulfate or intravenous, subcutaneous, or oral beta mimetic therapy. Accurate gestational dating was defined as knowledge of the most recent menstrual period with confirmation by first-trimester pelvic examination or ultrasound evaluation at less than 28 weeks of gestation. Criteria for exclusion included the presence of congenital anomalies, placenta previa, recent (within 24 hours) intercourse, or previous pregnancies terminated before term because of maternal hypertension, fetal growth retardation, or fetal distress. Patients with preterm rupture of membranes or preterm contractions were tested for cervical and vaginal fetal fibronectin only once on arrival at the hospital.
Control Patients
One hundred sixty-three patients receiving prenatal care in the Mount Sinai Hospital obstetrical clinic who met none of the exclusion criteria and had no complications of pregnancy (preterm contractions, preterm rupture of membranes, or vaginal bleeding) also underwent evaluation for the presence of cervicovaginal fetal fibronectin. These control patients were tested an average of four times between 5 and 40 weeks of gestation. To determine whether maternal plasma contained fetal fibronectin, plasma concentrations were measured in a cross-sectional fashion in blood collected in 5 mM EDTA obtained from 144 patients with uncomplicated pregnancies during the first (n = 14), second (n = 40), or third (n = 90) trimester. Fetal-fibronectin concentrations were measured in amniotic fluid in four patients undergoing amniocentesis to assess fetal pulmonic maturity between 36 and 38 weeks of gestation. First-voiding urine samples were obtained from four infants born at term.
Sampling and Assay
After the patients had given informed consent, fetal fibronectin was assayed by taking samples of both the cervical and posterior vaginal forniceal mucus with separate Dacron swabs during examination with a sterile speculum. Each swab was left in place for approximately 10 seconds and then withdrawn and placed in 750 μu.1 of sample buffer. Since the Dacron swab held 150 μl of fluid when saturated, the approximate dilution of cervicovaginal secretions in the buffer was 1 to 5. Samples of amniotic fluid, urine, and plasma were assayed directly. Concentrations of fetal-fibronectin antigen were measured with a sensitive immunoassay (ROMCheck, Adeza Biomedical, Sunnyvale, Calif). This assay used the fetal-fibronectin—specific monoclonal antibody FDC-6.3 4 5 The assay also used a goat antihuman plasma fibronectin IgG conjugated to alkaline phosphatase and a phenolphthalein monophosphate substrate. The absorbance of each standard and sample was determined in duplicate at a wavelength of 550 nm with an automated microtiter-plate reader, and fetal-fibronectin concentrations were derived from the SoftMax software program (Molecular Devices, Menlo Park, Calif.). The interassay and intraassay errors were less than 10 percent, and fetal fibronectin was detected in the range of 0.02 to 4 μg per milliliter. Values greater than 0.05 μg per milliliter were considered positive after post hoc analysis. The results of the fetal-fibronectin assays were not available to the clinicians.
Immunohistochemical Staining for Fetal Fibronectin
To assess the distribution of fetal fibronectin in women with uncomplicated pregnancies and account for the presence of cervicovaginal fetal fibronectin in patients who subsequently had preterm deliveries, a detailed immunohistochemical analysis of the placenta and external membranes was undertaken. Specimens for analysis were obtained from the Mount Sinai Department of Pathology, among them samples from women with term and preterm singleton and twin gestations (n = 14), uterine-curettage specimens from women with ectopic pregnancies (n = 2), and fetal tissues from a second-trimester postmortem examination.
All the tissues had been routinely placed in 10 percent formalin for three hours, then sequentially dehydrated and embedded in paraffin wax according to standard laboratory protocol. Stored paraffin blocks were selected, cut into 5-μm sections, and placed on glass slides coated with 1 percent poly-D-lysine. After removal of the paraffin in xylene and graded ethanol the specimens were rinsed in deionized distilled water and exposed to 1 percent hydrogen peroxide. Selected specimens were preincubated with 0.1 percent pepsin (porcine-stomach mucosa, Sigma, St. Louis) in 0.01 N hydrogen chloride at 37°C for 20 minutes to minimize the potential for masking of fibronectin antigen.8 Immunoperoxidase staining was then carried out with a detection system for the avidin–biotin–peroxidase complex (Vector Laboratories, Burlingame, Calif.). Primary antiserum included FDC-6 from mouse ascites (4 mg of protein per milliliter; Adeza Biomedical) diluted 1 to 2000; affinity-purified goat polyclonal antitotal fibronectin (1 mg per milliliter of stock) (Adeza Biomedical) diluted 1 to 1000; monoclonal antibodies to low-molecular-weight cytokeratin (Dakopatts, Carpentaria, Calif.) diluted 1 to 5, which stain all trophoblasts but not decidual cells9; and monoclonal antibodies to vimentin (Dakopatts) diluted 1 to 5, which stain decidual cells but not trophoblasts.9 Control assays were performed by replacing the primary antibodies with normal serum from the same species or with FDC-6 preadsorbed with excess immunoaffinity-purified fetal-fibronectin antigen (Adeza Biomedical).
Statistical Analysis
We used stepwise multivariate logistic-regression analysis to evaluate the association between cervicovaginal fetal-fibronectin status and preterm delivery while controlling for potential confounding variables. Odds ratios were calculated from the regression coefficients. All data were analyzed with BMDP statistical software (BMDP, Los Angeles). AP value of less than 0.05 was considered to indicate significance (two-tailed analyses were used, with Fisher's exact test and the Kruskal—Wallis test). All concentrations are reported as means ±SD.
Results
Clinical Studies
Control Patients
Figure 1Figure 1
Percentage of Cervical and Posterior Vaginal Forniceal Samples with Fetal Fibronectin, According to Week of Gestation, in Patients with Uncomplicated Pregnancies Who Delivered at Term. shows the frequency of cervical and vaginal fetal-fibronectin levels above 0.05 μg per milliliter in 588 samples from the patients with uncomplicated pregnancies. Before 22 weeks of gestation, 24 percent of the cervical samples (70 of 290) and 17 percent of the vaginal samples (50 of 291) were positive for fetal fibronectin. After 37 weeks or more, 32 percent of the cervical samples (10 of 31) and 17 percent of the vaginal samples (5 of 30) contained fetal fibronectin. Between week 21 and week 37, only 4 percent of the cervical samples (11 of 267) and 3 percent of the vaginal samples (9 of 267) were positive for fetal fibronectin. The mean concentrations of cervical and vaginal fetal fibronectin in these latter samples were 0.26±0.22 μg per milliliter and 0.27±0.23 pg per milliliter, respectively. The mean maternal plasma fetal-fibronectin concentrations were 1.3±0.7 pg per milliliter, 2.0±2.3 pg per milliliter, and 3.5±2.2 μg per milliliter, in the first, second, and third trimesters, respectively. Maternal plasma fetal-fibronectin concentrations correlated with the length of gestation (R = 0.41, P<0.01).Study Patients
There were no statistically significant differences in maternal age, gravidity, parity, or race between the patients who were positive and the patients who were negative for cervical or vaginal fetal fibronectin in either the group with preterm rupture of membranes or the group with preterm contractions.
Of the patients with clinical evidence of preterm rupture of membranes, 93.8 percent had cervical and vaginal fetal fibronectin. The mean concentrations of fetal fibronectin in cervical and vaginal secretions were 5.5±11.4 μg per milliliter and 6.9±11.1 pg per milliliter, respectively. Although these values are only relative measures of cervicovaginal levels of fetal fibronectin, given the variability in the sampling technique and the fivefold dilution of the swab specimens in sample buffer, they were consistent with fetal-fibronectin levels measured in amniotic fluid at term (27.1±17.3 μg per milliliter). The mean interval between rupture and delivery was 2.1 days in the 61 patients with cervicovaginal fetal fibronectin, as compared with 21 days in the 4 patients with preterm rupture of membranes who had no evidence of cervicovaginal fetal fibronectin. This difference suggests that the patients without cervicovaginal fetal fibronectin represented a distinct clinical subgroup.
Of the 117 patients presenting to the hospital with uterine contractions but without evidence of preterm rupture of membranes, 51.3 percent delivered before 37 weeks of gestation (Table 1Table 1
Association between Cervical or Vaginal Fetal Fibronectin and Preterm Delivery in Patients with Preterm Uterine Contractions.*). The patients with preterm contractions who had cervical or vaginal fetal fibronectin were far more likely to deliver before term than were the patients without fetal fibronectin (83.1 vs. 19.0 percent, P<0.01 by Fisher's exact test). Conversely, the patients delivering before term were far more likely to have fetal fibronectin than those delivering at term (81.7 vs. 17.5 percent, P<0.01). Among the patients positive for fetal fibronectin who delivered before term, the mean concentrations of fetal fibronectin in cervical and vaginal secretions were 2.2±5.7 μg per milliliter and 2.3±5.7 μg per milliliter, respectively, as compared with 1.5±3.4 μg per milliliter and 0.4± 1.0 μg per milliliter, respectively, among the patients positive for fetal fibronectin who delivered at term. Post hoc adjustments of the fetal-fibronectin threshold to 0.025 and 0.075 μg per milliliter were associated with reduced discriminatory power (sensitivity and specificity, 81.7 and 78.3 percent, and 77.7 and 82.5 percent, respectively).A stepwise multivariate logistic-regression model was devised to examine the independent contributions of cervicovaginal fetal fibronectin, cervical dilatation and frequency of contractions on admission, grossly apparent vaginal bleeding, tocolytic therapy, and gestational age at sampling to the prediction of preterm delivery. This model demonstrated that only cervicovaginal fetal fibronectin (odds ratio, 4.28; 95 percent confidence interval, 2.29 to 8.04; F = 22.0), cervical dilatation (odds ratio, 2.93; 95 percent confidence interval, 1.38 to 6.21; F = 8.3), and tocolytic therapy (odds ratio, 2.33; 95 percent confidence interval, 1.23 to 4.40; F = 7.14) were significant independent predictors of preterm delivery. Vaginal bleeding (F = 0.33, P = 0.57), frequency of contractions (F = 1.79, P = 0.18), and gestational age at sampling (F = 1.08, P = 0.40) were not significant predictors of preterm delivery.
No correlation was found between the presence of cervicovaginal fetal fibronectin and cervical dilatation (R = 0.04, P>0.05). Furthermore, cervicovaginal fetal fibronectin continued to identify risk of preterm delivery among patients with preterm contractions who had ≤2 cm of cervical dilatation when the secretions were sampled, with a sensitivity of 71.4 percent (20 of 28) and a specificity of 83.7 percent (41 of 49). Given the presence of fetal fibronectin in maternal plasma, we excluded all 30 patients with preterm contractions who had bloody cervicovaginal specimens on gross examination. In this setting, fetal fibronectin remained an excellent discriminator of risk for preterm delivery, with a sensitivity of 79.4 percent (27 of 34) and a specificity of 82.7 percent (43 of 52).
Tables 2Table 2
Outcomes of Pregnancy in Patients with Preterm Contractions, According to Fetal-Fibronectin Status and Time of Delivery.* and 3Table 3
Maternal Antepartum and Postpartum Characteristics and Neonatal Outcomes, According to Fetal-Fibronectin Status and Time of Delivery.* show sampling data and the characteristics of the patients with preterm contractions and their newborns, according to both fetal-fibronectin status and time of delivery. Patients with cervical or vaginal fetal fibronectin who delivered before term had a greater degree of cervical dilatation and were more likely to have antepartum bleeding, peripartum infections, and a neonate with respiratory distress syndrome or perinatal death than patients in the remaining groups. In these patients there was also a shorter interval between sampling and delivery than in the patients negative for fetal fibronectin who delivered before term. None of the patients who were negative for fetal fibronectin who delivered before term had peripartum infections or morbidity in the newborn.Immunohistochemical Studies of Fetal Fibronectin
Immunohistochemical studies revealed the highly specific localization of fetal fibronectin in the extracellular matrix of the decidua basalis adjacent to the intervillous space (cytotrophoblastic shell) (Fig. 2Figure 2
Immunohistochemical Studies of Fetal Fibronectin.A) and the cytotrophoblastic cell columns. The cells surrounded by fetal fibronectin had intense staining for cytokeratin but not for vimentin, a pattern consistent with that of extravillous cytotrophoblasts9 (data not shown). The villous trophoblasts stained for cytokeratin but not for vimentin or fetal fibronectin. Decidual cells distant from the cytotrophoblastic shell, uterine decidua from ectopic gestations, and villous endothelium and fibroblasts stained for vimentin but not for cytokeratin or fetal fibronectin.Analyses of membrane-roll preparations revealed a more diffuse distribution of fetal-fibronectin staining in the membrane extracellular matrix than in the placenta. Staining for fetal fibronectin extended from the attached decidua to the basement membrane of the amnion (Fig. 2B). Chorionic trophoblasts showed intense intercellular staining for fetal fibronectin, intense intracellular staining for cytokeratin, and no staining for vimentin (data not shown). The most intense staining for fetal fibronectin was in the deciduafree, fused chorionic trophoblastic layer of dichorionic placental membranes.
In fetal tissues, fetal fibronectin was identified in hepatocytes and in the cytoplasm of renal collecting tubules. Fetal urine, however, is not a source of amniotic-fluid fetal fibronectin at term, since immunoassays of first-voided urine in newborns failed to detect fetal fibronectin. Positive staining for fetal fibronectin was consistently eliminated when the primary antibodies were replaced by normal serum or FDC-6 preadsorbed with excess fetal fibronectin.
In contrast to the pattern of staining for fetal fibronectin, there was diffuse staining for total fibronectin throughout the decidua, villous stroma, syncytiotrophoblasts, amnion, chorion, and fetal extracellular matrix.
Discussion
It was not surprising to detect fetal fibronectin in the cervicovaginal secretions of patients with preterm rupture of membranes, given the high levels present in amniotic fluid. However, in patients with intact membranes who were admitted to the hospital to rule out preterm labor, the presence of cervicovaginal fetal fibronectin made it possible to distinguish between those with irrelevant uterine contractions and those at true risk for preterm delivery.
Given the finding of an amniotic-fluid protein in the cervix and vagina of patients with preterm labor and apparently intact membranes, one potential source of cervicovaginal fetal fibronectin could be the occult leakage of amniotic fluid across injured membranes. This mechanism is doubtful, however, since transfer of the fetal-fibronectin glycoprotein (molecular weight, 450,000 or more) is unlikely without the passage of substantial quantities of water and proteins of lower molecular weight. Moreover, none of the patients with preterm contractions had more than one criterion of membrane rupture, and the mean concentrations of cervical and vaginal fibronectin were significantly lower in the group with preterm contractions than in the group with membrane rupture (P = 0.05 and 0.006, respectively, by t-test). Membrane rupture thus appears to be an unlikely source of cervicovaginal fibronectin in patients with clinically intact membranes who deliver before term.
An alternative source of cervicovaginal fetal fibronectin in patients who have preterm labor and apparently intact membranes can be surmised from the immunohistochemical localization of fetal fibronectin to the area where the placenta and its membranes meet the uterine wall. This localization paradoxically suggests that fetal fibronectin plays a critical part both in maintaining contact between the uterus and the placenta and its membranes and in facilitating the physiologic separation of the placenta from the uterus after the fetus has been delivered. The enhanced glycosylation of placental fibronectin has been shown to reduce substantially its binding affinity for other components of the extracellular matrix,10 a biochemical property compatible with this dual role. Since preterm delivery is invariably preceded by separation of the chorion from the decidual layer of the lower uterine segment, the reduced binding affinity of fetal fibronectin may facilitate this separation and permit release of the protein into the cervicovaginal secretions. Alternatively, fetal fibronectin may be released into the cervix and vagina in response to inflammation-mediated proteolysis of the chorionic extracellular matrix. Consistent with this latter hypothesis is the in vitro evidence of fibronectin release from the extracellular matrix of fetal membranes exposed to activated neutrophils.6
Its frequent appearance at term suggests that fetal fibronectin may be a marker for labor in general and that term and preterm labor are accompanied by common changes in the homeostasis of the membrane extracellular matrix or by the separation of the chorion from the uterine decidual layer. The disappearance of cervicovaginal fibronectin between 16 and 20 weeks of gestation parallels the fusion of the chorion and adjacent decidua capsularis remnant with the decidua parietalis of the uterine wall. This fusion presumably creates a seal that prevents the further release of chorionic fetal fibronectin.
We conclude that the release of fibronectin bearing the oncofetal domain into the cervicovaginal secretions of pregnant women during the second and third trimesters can be used to distinguish between symptomatic patients who will deliver prematurely and those who will deliver at term. Although it is possible that identifying these patients could lead to meaningful therapeutic interventions, the mere identification of patients at risk does not necessarily result in improved outcomes.2 For the finding to be clinically useful, subsequent studies must confirm that the presence of cervicovaginal fetal fibronectin can identify asymptomatic patients who are at risk for preterm delivery at a point in the pathologic process that is amenable to therapy.
Supported by a Kennedy-Dannreuther Fellowship from the American Association of Obstetricians and Gynecologists Foundation and a Revson Foundation Fellowship to Dr. Lock wood, and by Adeza Biomedical.
We are indebted to Dr. Nelson Teng for his guidance and support; to Rosemary Wein, R.N., Pamela Rumney, R.N., Donna Beiter, R.N., and Drs. Ziaodong Zhou and Paul Kaplan for their expert technical assistance; and to the resident physicians of the participating centers.
Source Information
From the Department of Obstetrics, Gynecology and Reproductive Science and the Department of Pathology, Mount Sinai School of Medicine, New York (C.J.L., M.R.D., K.D.S., S.N.T., L.D.); Adeza Biomedical, Sunnyvale, Calif. (A.E.S., D.C., L.J.); and the Department of Obstetrics and Gynecology, University of California at Irvine, Irvine (A.E.S., T.J.G.). Address reprint requests to Dr. Lockwood at the Department of Obstetrics, Gynecology and Reproductive Sciences, Mount Sinai School of Medicine, I Gustave Levy Pl., New York, NY 10029–6574.
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